Abstract: The unstable genomes among the diploid Solanum species viz: Solanum macrocarpon, S. aethiopicum, S. gilo, S. anguivi and the varieties of S. melongena are indicative of progressive evolutionary changes. The high occurrence of chromosome bridges, clumps unequal anaphase chromosomes and faulty cytokinesis led to the production of poor quality pollen. However, bivalents were regular in S. torvum, S. erianthum and the tetraploid S. scabrum while their mitotic chromosomes were small-sized and symmetrical. The diploids with unstable genomes were cosmopolitan and found in the four ecological zones while the regular and normal diploids were limited in their distribution to the savanna, arid and semi arid. However, the tetraploid S. scabrum was restricted to the rainforest of Southern Nigeria. The colchicine induced tetraploid and its intermediate aneuploids suggest the likely origin of the natural polyploids. Consequently, the impact of genome changes was revealed in the evolution of different adaptive features and species ability to occupy new environment.
INTRODUCTION
Meiosis is a complex but regulated cellular event that ensures continuity of life. Constant genomic changes through specific gene interactions (Kumar and Bennetzen, 1999; Bennetzen, 2002) and the synthesis of new cellular components (Kimura et al., 1999) such as required for the new adaptive complexes are essential for species survival in constantly changing environment (Cai and Xu, 2007). The production of viable gametes for next generation of individual species is predicated on normal and harmonious meiosis (Pagliarini, 2000) and dependent on nuclear content, cytoplasmic inclusions and including lots of abiotic factors (Porch and Jahn, 2001; Erickson and Markhart, 2002). The emergence of novel characters is a consequence of several cytogenetic interplay that regulates gene expression pattern (Liu and Wendel, 2003; Levy and Feldman, 2004) and capable of producing new genotypes within a population (Oyelana and Ogunwenmo, 2009a).
The production of gametes with inherent numerical or structural chromosome variations have been well documented (Bretagnolle and Thompson, 1995; Page and Hawley, 2003; Kato and Palmer, 2003) and the expanded genomes in the emerging polyploids are maintained on a somewhat different cytogenetic processes (Bennetzen and Kellog, 1997; Xu and Joppa, 2000) to ensure stability. These several meiotic processes including methylation and epistasis (Doyle et al., 2008; Leitch and Leitch, 2008) and loss of sequences of DNA (Raina et al., 1994; Eilam et al., 2009) subsequently ensure the production of balanced gametes. This is a critical step in polyploid speciation (Rieseberg and Willis, 2007; Rezaei et al., 2010) and the basis for the functionality of polyploid genomes (Carroll, 2000; Chen, 2007) and their colonization and success in new environment (Soltis et al., 2003; Brochmann et al., 2004).
The population analyses of Solanum spp. in Nigeria including similar tropical environment reveal a mix population of cytotypes viz.: diploids (2n = 24) (Oyelana and Ugborogho, 1997; Oyelana, 1997), triploids (2n = 36) (Bir and Neelam, 1984; Okoli, 1988), group of aneuploid numbers (Omidiji, 1983; Govindarajan and Vijayakumar, 1986) and tetraploids (2n = 48) (Ceschmedjiev, 1976; Oyelana, 2005) growing in close proximity and constantly exchanging genes. This gives credence to a constantly expanding genome for members of this genus (Ugborogho and Oyelana, 1999; Oyelana, 2005) and the ease by which polyploids are formed following hybridization.
A number of polyploid hybrids including triploids (Gavrilenko et al., 1999), Colchicine induced tetraploids (Oyelana and Ogunwenmo, 2005), pentaploids (Oyelana and Ogunwenmo, 2009b) and hexaploids (Oyelana et al., 2009) were successfully generated and were able to compete favourably alongside the natural populations of diploids and tetraploids. Hijmans et al. (2007) reported similar mixed population of diploids, triploids tetraploids and pentaploids in Central and South America. The genus Solanum is diversed morphologically and are mostly shrubs to small trees, annual and rarely perennial (Omidiji, 1983; Gbile, 1985). The different species express variation and rare overlaps in growth habit and distribution (Lester and Seck, 2004) across the four ecological zones in Nigeria in spite of similar and closely related genomes (Okoli, 1988; Oyelana, 2005). Some species are habitat specific and inhabit the mountain zones, particularly the highlands of Mambilla, Obudu Vogel peak and Jos Plateau across the Nigerian savanna and arid belt while others are Lowland species (Heine, 1963; D’Arcy, 1979). The continuous morphological variations, near similar genomes, overlaps in cytological features (Gbile, 1985; Edmonds, 1986; Knapp, 1991) and emergence of new cytotypes (polyploids) could be attributed to the extensive hybridization and breeding programmes involving a number of past intra and interspecific crosses (Marfil et al., 2006; Oyelana and Ugborogho, 2008) aimed at improving species productivity and agronomic qualities.
The significance of meiosis in providing the platform for the synthesis of both morphological and physiological features essential for species adaptation in new environment through a set of intrinsic network of gene regulatory mechanism is the focus of this review. Consequently, the distribution pattern of eight Solanum species involving ten taxa of different genomic constitution Table 1 is analysed to establish any correlation (s) between meiotic behaviour and the performance or productivity of the different species across the four different ecological zones in Nigeria.
MEIOTIC BEHAVIOUR AND STRUCTURAL CHANGES IN THE SPECIES’ CHROMOSOMES
The diploid and tetraploid chromosome numbers of 2n = 24, 48 (Omidiji, 1983; Okoli, 1988; Oyelana and Ugborogho, 1997; Oyelana, 2005) revealed 12 and 24 bivalents, respectively for the diploid and Tetraploid species However, the variants: n = 10, 13, 18 and 22 (Ceschmedjiev, 1976; Labadie, 1976; Oyelana and Ugborogho, 1997) and 2n = 20, 22, 26 and 28 (Gill, 1975; Crompton and Bassett, 1976; Leslie, 1978; Bir et al., 1978; Oyelana, 2005) constitute the aneuploid cytotypes particularly among the diploid populations of Solanum. macrocarpon, S. gilo, S. aethiopicum, S. anguivi and the varieties of S. melongena.
| Table 1: | Species cytological traits and ecological distribution |
| Adapted from Oyelana and Ugborogho (1997) | |
The few triploids including S. nigrum (Vasudevan, 1975) and hexaploid in S. erianthum (Crompton and Bassett, 1976; Leslie, 1978) have been reported. Meiosis was normal with regular bivalents in S. erianthum, S. torvum and the two sub species S. scabrum. Their somatic chromosomes length were found as small-sized (1.29-1.88μm), symmetrical and mostly metacentric to submetacentric. The homomorphic pairs revealed 6 long and 6 short and all 24 short chromosomes, respectively for the two diploids (S. erianthum and S. torvum) and the tetraploid (S. scabrum) (Oyelana, 2005).
The deviation from the basic chromosome number and the existence of aneuploid in S. macrocarpon, S. gilo, S. anguivi, S. aethiopicum and S. melongena suggest extensive meiotic irregularities. The unstable genomes and the high occurrence of diads and triads may have generated the 2n gametes reported for some members of this group (Oyelana and Ugborogho, 1997; Oyelana, 2005). Lagging and unequal anaphase chromosomes as commonly observed in S. aethiopicum and the varieties of S. melongena may have been responsible for the production of diads and triads through faulty cytokinesis in these species.
Rezaei et al. (2010) attributed the production of polyads in wheat to this phenomenon. Lyrene et al. (2003) explained that the occurrence of unreduced gametes from faulty cytokinesis may constitute a major mechanism for the emergence and wide spread of polyploids. Chromosome breaks and shift in centromeric positions may have produced the large (2.33-3.52μm) and asymmetrically shaped chromosomes in S. melongena, S. macrocarpon, S. anguivi and S. gilo (Oyelana, 2005). Genome arrangement involving relocation of chromosome segments equally gave rise to asymmetrical chromosomes in Hepatica nobilis var. pubescens (Weiss-Schneeweiss et al., 2007).
Evidently, the pachytene chromosomes revealed inversion loops in S. aethiopicum, S. melongena ‘Melongena’, S. anguivi and S. macrocarpon. A few x-shaped chromosomes in S. aethiopicum and S. melongena ‘Golden’ suggests possible chromosome inversion and segment duplication in these diploid species as mentioned by Oyelana and Ugborogho (1997). Consequently, the emergence of subtelocentric chromosomes in this second group of diploid species (Oyelana, 2005) appears a recent development and suggesting that the metacentric chromosomes are primitive features in members of this genus as observed in the first and third groups of species.
This feature (Karyotype) has severally been used to assess phylogenetic relationships between Angiosperm species (Pandit and Badu, 1993; Pringle and Murray, 1991). The presence of isolated chromosomes may further explain the inclusion of foreign gene through past hybridization efforts (Oyelana and Ugborogho, 1997) and the source of genomic instability in members of this second group of diploids.
MEIOSIS, SPECIES REPRODUCTIVE SUCCESS AND VIGOUR
Excessive multivalents and chromosome clumps are known to generate illegitimate meiotic recombination (Cai and Xu, 2007) thereby counteract genome expansion and produce unequal cross-over (Wicker et al., 2003; Ma et al., 2004). These two major processes may have constituted the major force ‘downplaying’ the potentials inherent in most diploid Solanum species The hybrids (2n = 24) from S. gilo×S. aethiopicum (Ugborogho and Oyelana, 1999) had no fruits while the hexaploid hybrid (2n = 72) of S. melongena ‘Golden’ (2n = 24)×S. scabrum sub species scabrum (2n = 48) was morphological similar to the male parent and without any special agronomic feature of economic values (Oyelana et al., 2009). Also the inherent chromosome mutations (Ugborogho and Oyelana, 1999) existing in the genomes of both or either parent species may have downplayed the potential of an expanded genome in this hexaploid hybrid.
The increasing number of polyploids in S. tuberosum was linked to the occurrence of 2n gametes resulting from faulty asynapsis and desynapsis (Ramanna, 1983), abnormal spindle orientation at the second division (Veilleux et al., 1982) and abnormal cytokinesis (Mok and Peloquin, 1975). The presence of a modulating mechanism worked through these genomic changes and significantly lowered pollen viability to 8 and 49.7%, respectively in the F1 diploid hybrid and its backcross from S. giloxS. aethiopicum compared to the 83.8 and 90% in both male and female parents. The 71 and 97.4% pollen viability in the male and female parents S. melongena ‘GoldenxS. scabrum sub species scabrum was reduced to 38.2% in the hexaploid hybrid and these two hybrids produced intermediate values for most of the morphological features (Ugborogho and Oyelana, 1999; Oyelana et al., 2009).
Meiotic abnormalities and consequent low meiotic indexes (few dividing cells) were equally observed in Adesmia ciliate (Tedesco et al., 2002) and adduced for the low pollen fertility. Equally the low percentage of pollen fertility in certain hybrids (Bione et al., 2000) was attributed to meiotic abnormalities.
Chromosome arm rearrangement was adduced for the reduction of fertility in hybrids involving interspecific crosses among certain taxa of the genus Draba (Skrede et al., 2008). A possible large dosage of recessive alleles from cross-over of genes and exchange of chromosome segments between homologous pairs may have contributed to the reduction in fertility in this second group of diploids. The high rate of multivalents and chromosome clumps in these diploid species equally help confirm the extent of homogeneity of genomes in this group of species.
The low pollen fertility in two of the thirteen species of Leucaena (Boff and Schifini-Wittmann, 2002) was attributed to the degree of multivalent chromosomes and chromosome stickiness. Jiang et al. (2011) demonstrated that in Epimedium acuminatum, E. pubescens, E. chlorandrum, E. davidii and E. ecalcaratum with 11, 8.6, 31.6, 38.3 and 3.3% meiotic abnormalities revealed a corresponding 82, 87, 80, 76.6 and 90% pollen fertility.
The occurrence of diads and triads has been linked to poor quality pollen in Solanum species and the subsequent small sized fruits and low number of seeds in fruits (Oyelana and Ogunwenmo, 2009a,b). Mendes-Bonato et al. (2001) and Caetano-Pereira and Pagliarini (2001) linked the occurrence of sterile pollen to the formation of diads, triads and polyads and which often manifests in reduction of the number of seeds in fruits (Stone et al., 1995).
The reduction in the sizes of most morphological features including number and dimension of leaves in the tetraploid S. scabrum shows an unexpected departure from the predicted additive effects of genome doubling. An epigenetic modulating mechanism may have helped restored a diploid-like behaviour and appearance in this tetraploid. Soltis et al. (2007) observed a number of natural autopolyploids which were typically morphologically similar to their diploid progenitors. However, this natural autotetraploids (the two sub species of S. scabrum) were resistant to the larvae of Papilio polyxenes (Lepidoptera) and adults of Toxoptera graminum (Homoptera) (Oyelana, 1997). This special feature offered them a competitive advantage over their diploid relatives found growing in the rainforest where these insects were prevalent and according to Felber (1991) and Schranz and Osborn (2004), higher tolerance of stress and diseases allow polyploid plants to occupy new ecological niche and expand their geographical range.
MEIOSIS AND SPECIES GENOME UNDER DIFFERENT ENVIRONMENTAL CONDITIONS
Meiotic behaviour and estimate of pollen fertility help assess species potentials for reproductive success, genetic variability, biodiversity and survival in new environment (Boff and Schifini-Wittmann, 2002). The genomic instability in the second group of diploid species and their ability to be wide spread across the four eco-geographical zones of Nigeria over and above the other diploid and Tetraploid species (with much stable genomes but somewhat restricted distribution) may highlight the adaptability of genome in a new environment.
The whole process of meiosis is under some form of genetic and environmental control as explained by Porch and Jahn (2001), Sun et al. (2004) and Bajpai and Singh (2006). The temperature range of the typical savanna and semi arid zones may have impacted the processes of meiosis and gametogenesis in this second group of diploid species and which led to the production of the different aneuploid cytotypes. The unstable genome and irregular meiosis equally reflect in high number of asymmetrical chromosomes in these species They are less fertile and the number of hybrids produced from crosses involving these species was rarely fertile.
However, the first group of diploid species had smaller and symmetrically shaped chromosomes, highly fertile and readily produce viable hybrids. Fuzinatto et al. (2008) highlights the impact of high temperature and reduction in microspore development and they linked this to low pollen viability. According to Dafni and Firmag (2000) and Palma-Silva et al. (2008), the quantity and quality of pollen do not only ensure reproductive success but equally reflect the impact of environment on the process of gametogenesis and the success of any breeding programme.
The preponderance of (2n) gametes in the members belonging to the second group of diploids was attributed to meiotic abnormalities and faulty cytokinesis (Oyelana and Ugborogho, 1997). These two meiotic processes have been closely associated to the impact of the environment (Brochmann et al., 2004; Parisod et al., 2010) and were equally confirmed to trigger the production of (2n) gametes and subsequent development of polyploids.
The relative improvement in pollen viability, increase number of seeds and bigger fruits in the backcross progeny from S. giloxS. aethiopicum (Ugborogho and Oyelana, 1999) and the vigorous growth and bigger fruits in the pentaploid hybrid from the cross involving S. macrocarpon and its colchicine induced mutant (Oyelana and Ogunwenmo, 2005) help confirm the presence of a mechanism for genome repairs in these species This equally affirms that the inherent chromosomal abnormalities in this group are transient (environmental) and not as a result of permanent mutations.
IMPAIRED MEIOSIS, INCREASED ANEUPLOIDY AND HIGHER POLYPLOIDY
The members of the second group of diploids have under gone intense breeding and selection process for decades (Omidiji, 1983; Oyelana, 1997). They are majorly introduced plants which later became domesticated as these species constitute both the fruit and leafy vegetables among the different tribes in Nigeria and across the West Africa subregion (Gbile, 1985; Oyelana, 1997). The stress of adapting to new environment may have contributed to the observed genomic changes in members of this group. The first group of diploid and the tetraploid are more of natural species, less cultivated and grow in the wild. According to Parisod et al. (2010), the rate of autopolyploid formation increases with increasing environmental stress. Hence, the production of unreduced gametes through which polyploids are frequently formed is stimulated by environmental factors such as temperature, water and nutrient stress (Ramsey and Schemske, 1998).
The subsequent evolution of tetraploid genome in S. scabrum could be attributed to doubling of chromosome number via faulty cytokinesis and fusion of 2n gametes following crosses involving two distantly related diploid species Increased aneuploidy is equally an established phenomenon of evolutionary significance in this group. The preponderant of aneuploid cytotypes in the second group of diploids may continue to generate other higher levels of ploidies (Mehra, 1976; Aminuddin et al., 1985; Oyelana, 2005) as described in some reports. This is may be a driven force in the evolution of higher ploidy in this group of species.
Oyelana and Ogunwenmo (2005) successfully induced an autotetraploid mutant (2n = 48) from a diploid genome (2n = 24) and other aneuploid intermediates using different concentrations of colchicine. The regular bivalents and the small-sized chromosomes in the colchicine induced autotetraploid may help confirm S. scabrun as natural autotetraploid. Biscutella laevigata (an autotetraploid) showed successive downsizing of its genome (Konig and Mullner, 2005) while Rivero-Guerro (2008) established a corresponding decrease in chromosome length for most autopolyploids.
A number of triploids (Omidiji, 1983) and pentaploids (Sangowawa, 1986; Okoli, 1988) hybrids have been reported for the genus and were claimed to have arisen through the production of 2n gametes. Oyelana and Ogunwenmo (2009b) produced a pentaploid hybrid (2n = 60) by crossing an aneuploid mutant with its natural relative (2n = 24). The hybrid was vigorous, stout and highly fertile.
CONCLUSION
The haploid number viz: 10, 13 and 18 confirmed the preponderance of the aneuploid series with 2n = 20, 22, 26 and 28 and the tetraploid S. scabrum (2n = 24) as earlier reported. The seemingly low meiotic index in the colchicine induced mutants and the high meiotic irregularities helped trace the source of low pollen fertility in S. melongena, S. macrocarpon, S. anguivi and S. aethiopicum and the reason for poor hybrids from crosses involving members of this group. However, the viable and vigorous hexaploid hybrid (2n = 72) from S. melongenaxS. scabrum supports the evidence of the presence of genomic repair mechanism operating to restore normal meiosis and cytokinesis in some member species and subsequently the possibility for an expanded genome through successful hybridization. The diploid species with unstable genomes were broad-based (cosmopolitan) in distribution across the four ecological zones in Nigeria, the tetraploid S. scabrum was restricted to the rainforest zone while S. erianthum was predominant in the savanna and arid ecological zones.
ACKNOWLEDGMENTS
The senior author is grateful to the University of Lagos, Nigeria for support through grant No: AD/REG/4397 towards the successful completion of this project. We are also grateful to the staff of Biological gardens in both University of Lagos and Babcock University for helping to maintain the plants while in cultivation.