Synapsis in Robertsonian Heterozygotes and Homozygotes of Dichroplus Pratensis (Melanoplinae, Acrididae) and Its Relationship with Chiasma Patterns

Abstract

Dichroplus pratensis has a complex system of Robertsonian rearrangements with central-marginal distribution; marginal populations are standard telocentric. Standard bivalents show a proximal-distal chiasma pattern in both sexes. In Robertsonian individuals a redistribution of chiasmata occurs: proximal chiasmata are suppressed in fusion trivalents and bivalents which usually display a single distal chiasma per chromosome arm. In this paper we studied the synaptic patterns of homologous chromosomes at prophase I of different Robertsonian status in order to find a mechanistic explanation for the observed phenomenon of redistribution of chiasmata. Synaptonemal complexes of males with different karyotypes were analysed by transmission electron microscopy in surface-spread preparations. The study of zygotene and early pachytene nuclei revealed that in the former, pericentromeric regions are the last to synapse in Robertsonian trivalents and bivalents and normally remain asynaptic at pachytene in the case of trivalents, but complete pairing in bivalents. Telocentric (standard) bivalents usually show complete synapsis at pachytene, but different degrees of interstitial asynapsis during zygotene, suggesting that synapsis starts in opposite (centromeric and distal) ends. The sequential nature of synapsis in the three types of configuration is directly related to their patterns of chiasma localisation at diplotenemetaphase I, and strongly supports our previous idea that Rb fusions instantly produce a redistribution of chiasmata towards chromosome ends by reducing the early pairing regions (which pair first, remain paired longer and thus would have a higher probability of forming chiasmata) from four to two (independently of the heterozygous or homozygous status of the fusion). Pericentromeric regions would pair the last, thus chiasma formation is strongly reduced in these areas contrary to what occurs in telocentric bivalents. Dichroplus pratensis is a South American grasshopper, the geographic distribution of which covers most of Argentina, Uruguay and southern Brazil . A complex system of eight polymorphic and polytypic Robertsonian (Rb) fusions that involves the six large autosomes (L1 -L6) is superimposed upon the standard telocentric chromosome complement (2n = 18 + X$, 18 + XX?). Meiotic studies of a large number of Argentinian populations, demonstrated that the Rb fusions strongly affect chiasma frequency and distribution and thus, potential genetic recombination and meiotic orientation and segregation (BIDAU 1990(BIDAU , 1991(BIDAU , 1993(BIDAU , 1996BIDAU et al. 1991;MIROL and BIDAU 1991, 1992, 1994TOSTO and BIDAU 1991; MARTI 1995, 1998; MART^ and BIDAU 1995, 1998). An adaptive role of the fusions as potential reservoirs of coadapted supergenes through the creation of recombination-free chromosomal regions, has been pro-* Both authors are affiliated with the Consejo Nacional de Investigaciones Cientificas y Tknicas, Argentina. Rivadavia 191 7, (1033) Buenos Aires, Argentina.posed (BIDAU 1990(BIDAU , 1993(BIDAU ,...

A heterozygous paracentric inversion only detectable through Electron Microscopy, in the grasshopper Dichroplus pratensis (Melanoplinae, Acrididae)

“…Chiasma distribution of all telocentric bivalents is directly correlated to this synaptic behaviour: chiasmata are almost invariability proximal (P) and/or distal (D) and only very rarely, interstitial (I) (BIDAU 1990(BIDAU , 1991(BIDAU , 1996BIDAU et al 1991BIDAU et al , 2001MARTÍ and BIDAU 1995;MIROL and BIDAU 1994), and this features were also observed in males from the Manantiales population, except in chromosome L2 of the inverted male analysed in this paper (Fig. 1b, Table 3).…”

“…The observed distribution of chiasmata suggests that the synaptic behaviour the L2 bivalent in the inverted male is sequential during the progress of zygotene if there is a truly direct relationship between synapsis and the probability of chiasma formation (BIDAU 1993;MARTÍ and BIDAU 2001). Nevertheless, despite the observation of many nuclei at zygotene and pachytene (Table 1) with the LM, no evidence of pairing failure or chromosomal rearrangement was found.…”

“…The pairing behaviour of the L2 bivalent in D. pratensis was analysed in a previous paper; synapsis starts always from the ends which are attached to the inner nuclear envelope during zygotene and never from interstitial regions (MARTÍ and BIDAU 2001); this pairing pattern is common to all L telocentric bivalents. Chiasma distribution of all telocentric bivalents is directly correlated to this synaptic behaviour: chiasmata are almost invariability proximal (P) and/or distal (D) and only very rarely, interstitial (I) (BIDAU 1990(BIDAU , 1991(BIDAU , 1996BIDAU et al 1991BIDAU et al , 2001MARTÍ and BIDAU 1995;MIROL and BIDAU 1994), and this features were also observed in males from the Manantiales population, except in chromosome L2 of the inverted male analysed in this paper (Fig.…”

“…The male came from a population with high frequency of two Rb translocations (L1/L6 and L3/L4) and a very low frequency of a third one (L2/L5) (BIDAU and MARTÍ 2002). The inversion carrier was heterozygous for Rb translocations L1/L6 and L3/L4, and standard telocentric for L2 and L5 (MARTÍ and BIDAU 2001).…”

Effect of species-specific differences in chromosome morphology on chromatin compaction and the frequency and distribution of RAD51 and MLH1 foci in two bovid species: cattle (Bos taurus) and the common eland (Taurotragus oryx)

“…In the case of the bi-armed chromosomes in the common eland, a significant shift in the proximal MLH1 focus position towards the distal end of the SC arm was observed compared to bovine acrocentrics. Similar repression of male meiotic recombination in the proximal regions of bi-armed chromosomes was described in other bovid species (Vozdova et al 2013) as well as in humans (Lian et al 2008) and in mice and insects with Robertsonian fusions Martí and Bidau 2001;Dumas and Britton-Davidian 2002;Colombo 2013;Capilla et al 2014). This fact, together with the overall reduction in the number of the initial DSBs, may explain the significantly lower crossover density (the number of MLH1 foci per micrometer of the SC length) in the common eland compared to cattle.…”