Cytogenetic evidence of mixed disomic and polysomic inheritance in an allotetraploid (AABB) Musa genotype

Abstract

Background and aims: Edible bananas originated mainly from two wild species, Musa acuminata Colla (AA) and Musa balbisiana Colla (BB), and triploid cultivars with an AAA, AAB or ABB genome are the most widely used. In the present study, chromosome pairing affinities are investigated in a sterile AB Indian variety and in its fertile colchicine-induced allotetraploid (AABB) derivative to determine the inheritance pattern of the tetraploid genotype. The potential implications of interspecific recombination and chromosomal composition of diploid gametes for Musa improvement are presented.

Methods: The pairing of different chromosome sets at diploid and tetraploid levels was investigated through a combination of conventional cytogenetic and genomic in-situ hybridization (GISH) analyses of meiotic chromosomes, leading to a likelihood model of the pairing behaviour. GISH analysis of mitotic chromosomes was also conducted to reveal the chromosome constitution of hybrids derived from crosses involving the allotetraploid genotype.

Key results: Analysis of chromosome associations at both ploidy levels suggested that the newly formed allotetraploid behaves as a 'segmental allotetraploid' with three chromosome sets in a tetrasomic pattern, three sets in a likely disomic pattern and the five remaining sets in an intermediate pattern. Balanced and unbalanced diploid gametes were detected in progenies, with the chromosome constitution appearing to be more homogenous in pollen than in ovules.

Conclusions: Colchicine-induced allotetraploids in Musa provide access to the genetic background of natural AB varieties. The segmental inheritance pattern exhibited by the AABB allotetraploid genotype implies chromosome exchanges between M. acuminata and M. balbisiana species and opens new horizons for reciprocal transfer of valuable alleles.

Fig. 1.

(A). Chromosome pairing in ‘Kunnan’ (genome AB) at metaphase I assessed by conventional cytogenetic acetocarmine staining: pollen mother cell (PMC) showing 10II and 2I. Photograph taken under natural light, magnification: ×1250. (B) Schematic interpretation of (A).

Fig. 2.

Maximum log-likelihood of bivalents/cell in ‘Kunnan’ for models assuming two groups of Np and Nq chromosomes (Np + Nq = 11).

Fig. 3.

Distribution of bivalents per cell for ‘Kunnan’: observed (white) and under the model Np = 8 and Nq = 3 (black).

Fig. 4.

GISH study of chromosome pairing in ‘Kunnan 4x’ (genotype AABB). (A, B, C, F) Meiotic plates of ‘Kunnan 4x’. Superimposition of the three colours: DAPI staining chromosomes in blue, A genomic DNA revealed in green (FITC), B genomic DNA revealed in red (Texas red). (D) Higher magnification of part of (C): two homoeologous bivalents and one homologous balbisiana bivalent. (E) Schematic interpretation of (D). (G) Higher magnification of part of (B): homoeologous ‘frying pan’ trivalent (two chromosomes A + 1 chromosome B). (H) Schematic interpretation of (G). (I) Higher magnification of part of (F): homoeologous B/B/A/A/ tetravalent. (J) Schematic interpretation of (I). Arrows indicate bivalents and circles indicate multivalents. Magnification: ×1000.

Fig. 5.

(A). Chromosome pairing in ‘Kunnan 4x’ (genome AABB) at metaphase I assessed by conventional cytogenetic acetocarmine staining. (B) Schematic interpretation of (A). Photograph taken under natural light; magnification: ×1250.

Fig. 6.

Maximum loglikelihood (LH) of multivalents/cell in ‘Kunnan 4x’ for models assuming three groups of Np, Nq and Ns chromosomes (Np + Nq + Ns = 11) for Ns = 0 (plain line) or Ns = 3 (dotted line) values.

Fig. 7.

GISH analysis at mitotic metaphase in interspecific triploid Musa progeny: I9 [genotype AAB, derived from the cross ‘Kunnan 4x’ (AABB) × ‘IDN110’ (AAcv)] with 23 A + 11 B. (A) After superimposition of the three colours: B genomic DNA revealed in red (Texas red) and A genomic DNA revealed in green (FITC) and DAPI counter-stained chromosomes in blue. (B) Superimposition of DAPI (blue), used as DNA marker, and 45S rDNA probe revealed in green (FITC). Arrows indicate chromosomes with 45S rDNA. Magnification: ×1000.

Fig. 8.

GISH analysis at mitotic metaphase in interspecific triploid Musa progeny: E19 (genotype ABB) with 10 A + 23 B. (A) After superimposition of the three colours: B genomic DNA revealed in red (Texas red) and A genomic DNA revealed in green (FITC) and DAPI counter-stained chromosomes in blue. (B) Superimposition of DAPI and 45S rDNA probe revealed in green (FITC). Arrows indicate chromosomes with 45S rDNA. Magnification: ×1000.