Jones R N & Karp A (1986), “Introducing Genetics”, John Murray, p122-125
There are many exceptions to the rule in genetics. One of them is that not all inherited characters are determined by genes located in the nucleus. A small minority are controlled by genes located in cell organelles in the cytoplasm i.e. cytoplasmic genes, and these of course are exceptions to the chromosome theory of inheritance. Since they are extrachromosomal (i.e. outside the chromosomes), such genes are not subject to the normal rules of Mendelian heredity.
Leaf variegation in plants
One of the earliest and best known examples of cytoplasmic inheritance is that discovered by Correns in a variegated variety of the four-o'clock plant Mirabilis jalapa. Variegated plants have some branches which carry normal green leaves, some branches with variegated leaves (mosaic of green and white patches) and some branches which have all white leaves (Fig. 9.11).
Correns discovered that seed produced by flowers carried on the green branches gave progeny which were all normal green. It made no difference whether the phenotype of the branch which carried the flower used for pollen was green, white or variegated. Seed taken from white branches likewise gave all white progeny, regardless of the pollen donor phenotype. These of course died in the seedling stage. Seeds from flowers on variegated branches gave three kinds of progeny, green, white and variegated, in varying proportions; again regardless of the pollen donor phenotype. In other words, the phenotype of the progeny always resembled the female parent and the male made no contribution at all to the character. The effect is seen quite clearly in the difference which Correns found between reciprocal crosses:
The explanation for this unusual pattern of inheritance is that the genes concerned are located in the chloroplasts within the cytoplasm, not in the nucleus, and are therefore transmitted only through the female parent. In eukaryote organisms the zygote normally receives the bulk of its cytoplasm from the egg cell and the male gamete contributes little more than a nucleus. Any genes contained in the cell organelles of the cytoplasm will therefore show maternal inheritance. The leaf variegation is due to two kinds of chloroplasts: normal green ones and defective ones lacking in chlorophyll pigment. Chloroplasts are genetically autonomous (i.e. self-determining) and have their own system of heredity in the form of chloroplast ‘chromosomes’. These are small circular naked DNA molecules which carry genes controlling some aspects of chloroplast structure and function. A mutation in one of these genes, which affects the synthesis of chlorophyll as in Mirabilis, will therefore follow the chloroplast in its transmission and will not be inherited in the same way as a nuclear gene – Fig. 9.12 and Box 9.2.
Fig. 9.12 Inheritance of leaf variegation in Mirabilis jalapa. The character is controlled by cytoplasmic genes located in the chloroplast ‘chromosome’. Chloroplasts are self-perpetuating cell organelles and during sexual reproduction they are only transmitted through the cytoplasm of the egg cell, as undifferentiated protoplastids. They are not inherited through the pollen. The progeny of crosses therefore have the characters of the female parent and show maternal inheritance.
The other important point to note about the inheritance of chloroplasts is that they have no regular means of distribution, such as chromosomes do at mitosis, where they can be equally shared out to the daughter cells following division. A plant that begins life as a zygote containing a mixture of normal and mutant chloroplasts cannot therefore maintain the same mixture in all of its somatic cells. The two kinds of plastids are shared out randomly during cell division, according to the way they happen to be placed in the cytoplasm when it is partitioned. Some branches of variegated plants may therefore remain mosaic while others, by chance, may turn out to contain all white or all green chloroplasts in all of their cells. In a similar way the flowers on variegated branch may be of three kinds. Some will have egg cells with all green chloroplasts, some egg cells with all white and others will retain a mixture.
Box 9.2 The chloroplast genome
It is now known that the chloroplasts of plants carry their genetic information in the form of small circular DNA molecules, similar in size and form to the chromosomes of bacteria (Chapter 12). These DNA molecules contain genes which code for some of the proteins and RNAs used in chloroplast structure and function; and it is mutations in these genes which are most likely to be responsible for the leaf variegation effects described above. It must also be emphasised that chloroplasts are not totally independent of the nucleus in their heredity; most of their proteins are coded by nuclear genes, and mutations in these show normal Mendelian patterns of inheritance.
The DNA molecules which make up the chloroplast genome are ‘naked’ ones (Fig. 9.13) and bear no resemblance to the chromosomes of the nucleus , which are much larger and are composed of both protein and DNA (Chapter 2). The really surprising thing about the chloroplast DNA is the large number of copies which are present: up to 300 in a mature plastid. Since an average of 160 chloroplasts are present in a mesophyll cell of the mature leaf of a cereal such as wheat, this means that there may be as many as 48 000 chloroplast ‘chromosomes’ per mesophyll cell. The reason for this enormous redundancy of genetic information is unknown.
Fig. 9.13 Electron micrograph of a single circular molecule of chloroplast DNA (ctDNA) from the lettuce plant. The chloroplast ‘chromosome’ has a length of 155 000 base pairs of DNA. The small circles are ‘chromosomes’ of the virus fX174 (5370 nucleotides of DNA) which are included as a standard for calculating the size of the chloroplast ‘chromosome’. (Photograph kindly supplied by Dr Tristan Dyer, Plant Breeding Institute, Cambridge.)
Other examples of cytoplasmic inheritance
Leaf variegation due to chloroplast mutation is known in numerous other genera of plants: Epilobium and Pelargonium are two examples.
Many of the other examples of cytoplasmic inheritance, in a variety of species, appear to involve characters which are associated with functions of the mitochondria. They have to do with defects in growth and ATP energy metabolism. Well known cases include the ‘Poky’ (slow growing) mutants in the fungus Neurospora and ‘Petite’ mutants' in brewers yeast. The mitochondria, like the chloroplasts, are self-replicating organelles which contain their own genes and have a limited number of characters which are independent of the nucleus. They are transmitted mainly through the female line and mutations in their genes show the same pattern or maternal inheritance. Mitochondrial ‘chromosomes’ have a similar circular configuration of ‘naked’ DNA as chloroplasts. In a typical haploid yeast cell each of the mitochondria contains in the region of 50 small circular ‘chromosomes’.
Alleles of some genes interact with one another to give F1 phenotypes that show incomplete dominance or co-dominance. Their heterozygotes can be distinguished from the homozygotes and this produces a modified F2 phenotypic ratio of 1:2:1. Deviations from the 3:1 ratio also occur when one of the homozygous classes in an F2 is determined by a lethal gene. When two different genes control the same single character they may also interact in their expression and give rise to modifications of the Familiar 9:3:3:1 ratio. There are various modifications, depending upon the kind of interaction that occurs, but the transmission of the genes is normal and the nine genotypes expected with independent segregation are all present. Genes which are located outside of the nucleus, in cell organelles, behave differently in reciprocal crosses and show a pattern of maternal inheritance.