Spontaneous cell fusion during meiosis leads to unidirectional chromosome modification and B chromosome formation

In the last two years we have reported on our studies of maize from Sikkim, a popcorn of the Eastern Himalayas. During the study of the chromosome knob pattern a low frequency of abnormal meiosis was discovered in certain lines. Further investigation of pre-prophase to very early prophase stages discovered cell fusion of clonal pollen mother cells in the most precocious (early-to-flower) plants. It appears to us that these cells did not form a primary cell wall (possibly because of disruption induced by the very rapid photoinduction from long days of this short day tropical maize), and the naked cell membranes of cells in physical contact were subject to a process best described as fusion.

There is no question of the fusion and subsequent spontaneous increase in chromosome number (we have scored approximately 17,000 cells), but we are cautious about our observations because to our knowledge this is a first report. Following fusion, partially modified supernumerary chromosomes appear to stabilize their number and are known to be inherited through the third generation.

Plasmodiums of both meiotic cells and mitotic cells, plus somatic nurse cells, have been observed. Cell fusion composed of 3 or more cells always appears to abort, but the fusion of two cells resulted in a spectrum of products, from "stable" autotetraploids to the complete elimination of the invading complement and return to the 'normal' condition.

Most intermediate conditions involved one complement which appeared to differentially disintegrate while the other complement retained normal characteristics. Chromosome modification appeared to be unidirectional, with only the chromosomes from one complement undergoing partial to total modification and ultimately elimination. The conclusion that this modification-elimination was unidirectional is based on both direct microscopic observations and the recovery of normal karyotypes with supernumerary chromosomes in subsequent generations. We have stabilized lines through the F3 generation with 2n + 1B, 2n + 2B's, and 2n + 3B's, the first being the most frequent, following fusion in the original parent. The early photoinduction is inherited, and these selfed stocks are 30 to 45 days earlier than the original Sikkim collection in days to flowering. The day length response genes we assume to be on the normal complement.

We have observed these stabilized heterochromatic chromosomes to be no different from B chromosomes. Despite the considerable work done on supernumerary or B chromosomes, nothing is definitely known about their origin. One hypothesis, that B chromosomes have an origin from A chromosomes, has never been confirmed by direct cytological observations. In our observations, we have followed what we take to be the origin of a B-like chromosome following stabilization of the invading chromosome set or complement created by fusion. The complement that remains "normal" following fusion is the one that was in a slightly more advanced stage of meiosis. We have called this the invaded cell.

Cells which had acquired additional modified chromosomes and which appeared to have stabilized were found to fall into two categories. In the first category, the additional chromosomes were meiotically active. These cells were stable throughout meiosis. The second category was broader and included acentric fragments and additional chromosomes which failed to contract (and were defined as not meiotically active). In the latter case, these chromosomes were usually found in a pachytene-like state of contraction in cells where the other chromosomes were at more advanced and essentially 'normal' stages of meiosis. These unusual cells suggested to us that fusion has occurred before or at pachytene, and not at advanced stages.

Although the causes of cell fusion and unidirectional chromosome modification are not understood, a sufficient number of observations have been made to realize that this is a real phenomenon and conclusions can be drawn. This report has shown that additional chromosomes, whether modified or not, can arise spontaneously in cells as a result of cell fusion and/or chromosome transfer. Meiotic cells which have acquired extra elements express various degrees of stability, but can result in fertile gametes and subsequent spontaneous karyotypic modification in the next generation. Further, rapid unidirectional modification of chromosomes from cells of clonal origin suggests that there must be a complex and finely tuned chromosome/cytoplasm equilibrium. Lastly, the fact that partial elimination appears to lead to inherited modified chromosomes shows that the elimination mechanism need not be an all or none reaction, and that additional chromosomes, whether modified or not, having passed a certain threshold, will acquire normal cellular stability. We expect to publish these findings in full this year.

John P. Peeters and H. G. Wilkes


Please Note: Notes submitted to the Maize Genetics Cooperation Newsletter may be cited only with consent of the authors.

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