Heredity 71: 300-304 (1993)
Heterosis and nuclear DNA content in maize
D. P. BIRADAR AND A. LANE RAYBURN

Twenty-five F1 maize hybrids were analysed with respect to their nuclear DNA content. Twelve of the hybrids have been reported previously to have a low heterotic response while 13 have a high heterotic response. The nuclear DNA content of each F1 hybrid was compared with the midpoint DNA amount of its respective parents. In nine of the hybrids with the low heterotic response, the observed nuclear DNA amount exceeded the expected DNA amount by approximately 5 per cent. In 12 of the 13 hybrids that had a high heterotic response, the observed nuclear DNA amount was not significantly different from the expected DNA amount. These results demonstrate an association between heterotic response and nuclear DNA content inheritance in F1 hybrids of maize.

Introduction

Since its inception in 1909, the pure line hybrid concept developed by Shull has been extensively used in maize breeding (Shull, 1909). This breeding concept allows one to take advantage of the immense amount of heterosis that occurs in maize. Heterosis was defined by Shull (1911) as 'the superiority of heterozygous genotypes with respect to one or more characters in comparison with the corresponding homozygotes. Heterosis is the phenotypic result of gene interaction in heterozygotes and is thus confined (at least in maximal amount) to that state' (taken from Reiger et al., 1976). The degree of heterosis one observes appears to increase as the genetic similarities between the two parents decrease (East, 1936). Although heterosis is observed in maize as well as in a variety of other organisms, the specific basis of heterosis is not known.

Heterosis appears to be a complex phenomenon which is an important component of cross-fertilizing species (Elliot, 1958). Due to the complexity of heterosis, it may be difficult to ever determine the exact nature of heterosis. Pontecorvo (1955) stated '... the first steps for an understanding of heterosis... should be towards a better understanding of gene structure and action. Only then would the approach at the higher level of population genetics become illuminating'. While this statement appears restricted to studies of single (or quantitative) genes, implied in the statement is the importance of genome organization and its role in heterosis. Bennett (1984) reviewed quite extensively the role of nuclear architecture in F1 hybrids of plants. Nuclear organization, therefore, should not be ignored when studying heterosis.

Rayburn et al. (1993) determined the nuclear DNA content of several inbred lines and F1 hybrids in maize. They observed two distinct patterns of inheritance. In the first pattern, the nuclear DNA content of the hybrid is equivalent to the parental midpoint DNA amount. In the second pattern, the nuclear DNA amount of the hybrid was significantly higher than the parental midpoint. Included in the maize hybrids examined were hybrids that demonstrated high heterosis as well as hybrids that demonstrated low heterosis.

Observing two types of inheritance patterns in these hybrids leads one to speculate the influence of heterosis on these patterns. The objective of this research was to determine if the degree of heterosis observed in a hybrid may have an influence on the inheritance pattern in specific F1 hybrids.

Results

The five inbred lines were observed to have genome sizes ranging from 11.1 to 10.6 picograms (pg) per 4C nucleus (Table 1). These nuclear DNA contents are well within the range already observed for mid-western US inbred maize. The nuclear DNA content of the F1 hybrids ranged from 11.0 to 10.0 pg per 4C nucleus (Table 1). Again, this range of nuclear DNA contents was well within the norm for F1 maize hybrids examined previously. In all of the hybrids examined, all 10 plants examined were observed to cluster around their respective genome size.

Thirteen hybrids were examined which exhibited a high heterotic response. In 12 of the 13 hybrids, the observed nuclear DNA amount was not significantly different from the expected DNA content (Table 2). Only in the hybrid H100 X H102 was a significant deviation from the expected DNA amount found. In this hybrid, the nuclear DNA content was higher than expected. In the 12 hybrids which showed no significant difference from the expected, seven were observed to have a nuclear DNA content numerically higher than the expected, three hybrids were observed to have nuclear DNA contents numerically lower than expected and two hybrids had nuclear DNA contents equivalent to the expected value.

In the 12 hybrids with low heterotic response, a different trend was observed (Table 3). In nine of the 12 hybrids, the observed nuclear DNA content deviated significantly from the expected F1 DNA amount. In all nine hybrids, the nuclear DNA amount was higher than expected. In the remaining three hybrids, the observed DNA amount was also numerically higher than the expected although not statistically significant.

Discussion

Narayan (1988) hypothesized that interspecific hybrids showed genomic imbalance which may be associated with gain or loss in nuclear DNA amount. The theory presented indicated that the more closely related the genomes, the more stable the genomic organization would be. In maize, the opposite was observed. The hybrids which were the result of combining similar or closely related genomes resulted in amplifications of nuclear DNA sequences. When genomes which were more distantly related were combined, no deviations from the expected nuclear DNA amounts were observed. While four exceptions to these observations were noted, they all appeared to have special circumstances that could in part explain their nuclear DNA inheritance. Apparently, the maize plant has the ability to more precisely organize unrelated genomes without modification than closely related genomes in the hybrid nucleus. These results are contradictory to what one might have expected. However, maize, being a normal cross-fertilizing species, may have developed such a mechanism to deter inbreeding. The best performing, most stable hybrids would be those with the most stable genome organization as reflected by normal DNA inheritance.