Polyploidy and Diploidy: New Perspectives on Chromosome Pairing and Its Evolutionary Implications

Abstract

The last widely accepted classification of polyploidy recognized three major categories: autoploidy, segmental alloploidy, and true alloploidy. Criteria for recognizing these types were based largely on chromosome pairing in F1 hybrids, but until very recently there were no quantitative criteria to distinguish autoploids from segmental alloploids. This is theoretically possible, and Jackson and Casey (1982) and Jackson and Hauber (1982) have presented models and methods to quantitatively predict the frequencies of the different meiotic configurations in autotriploids through autooctoploids. The expected numbers of configurations then can be statistically tested for goodness of fit with observed data. Synthetic and natural autotetraploids have been shown to fit the models well. However, the exceptions that do not fit are of particular interest because they indicate the presence of Ph‐like (Pairing homoeologous) genes that cause fewer multivalents and more bivalents than expected in the autoploid models. The effect of Ph‐like genes at the nuclear level apparently involves placement of chromosome attachment sites on the nuclear membrane such that different genomes occupy slightly different sites. This would be far enough apart in true alloploids so that no pairing occurred in the original F1 hybrid. In true autoploids and normal diploids, homologues are equally close so that pairing obeys probability laws that make it possible to describe expected pairing events with appropriate models and equations. From the foregoing statements, one can deduce that the terms autoploid, segmental alloploid, and true alloploid need not and indeed should not be equated with results of crosses between any taxonomic levels. Rather, they represent conditions that can be attained by one or very few genes acting on nuclear membrane attachment sites. It is possible to deduce from hybrids at the diploid level the type of polyploid that can be obtained, and such data can have great agronomic value. A generally held dogma is that the inability of chromosomes to pair in F1 hybrids is due to considerable genetic divergence and perhaps numerous structural changes at the light microscope and/or ultrastructural level. Data from various sources show that this need not be true, and there is no reason to believe this is a factor in what has been called genome divergence in the classical sense. Genome divergence in terms of pairing ability can occur at the population level due to one or a few genes.

The BOY NAMED SUE Quantitative Trait Locus Confers Increased Meiotic Stability to an Adapted Natural Allopolyploid of Arabidopsis

“…Another hypothesis involves the development of a molecular pairing editor that rejects chromosomal pairing between chromosome partners that cross a certain threshold of divergence (Jackson, 1982;Stebbins, 1984). For example, in allohexaploid wheat, the Ph1 locus reduces homoeologous pairing between the three diverged sets of chromosomes of this allopolyploid (Griffiths et al, 2006) and is thought to encode a cyclin-dependent kinase pseudogene array that affects the timing of chromosome condensation (Yousafzai et al, 2010).…”

Cryptic homoeology analysis in species and hybrids of genus Zea

“…Additionally, they suggested that chromosome position is crucial in the meiotic pairing of homologous and homoeologous chromosomes, altering the arrangement of chromosomes in the nuclear membrane, and allowing the expression of cryptic genomic homology. Jackson (1982) described a model that explains the chromosome pairing and chiasma formation in homologous and homoeologous genomes, in which there is a genetic control of the specific binding site of chromosomes to the nuclear membrane, under the regulation of the Ph gene. Jackson and Murray (1983) demonstrated that the application of diluted colchicine solution to meiotic cells can break the genetic control of these genes, promoting the intergenomic pairing, and thus revealing the cryptic homology in polyploids.…”

Chromosome Numbers and Evolution in Anoda and Periptera (Malvaceae)

“…cristata is the strong preferential pairing observed at all ploidy levels and in one of the diploid/tetraploid hybrids, the other being more equivocal. De Wet and Harlan (1972), however, have pointed out the rapidity with which autoploids can establish normal pairing, and Jackson (1982) raises questions concerning traditional interpretations of polyploidy based on the kinds of pairing data available in this study. Whatever the extent of genomic differentiation in A. cristata, it is probably genic in character and represents little structural chromosomal differentiation.…”

“…The systematic treatments and nomenclature follow those of Fryxell (1974Fryxell ( , 1987. Jackson (1982Jackson ( , 1984 questioned characterizations of chromosomal pairing during meiosis and assumptions concerning autoploidy and alloploidy that are widespread in the taxonomic literature. While the relevance of Jackson's comments to this study are recognized, the cytological data available for Anoda and Periptera are those traditionally presented.…”