Male sterility in plants

Maternal Effects and Cytoplasmic Inheritance
Maternal effects
Cytoplasmic Inheritance Involving Dispensable Hereditary Units
Kappa particles in Paramecium
CO2 Sensitivity in Drosophila (sigma factor)
Organellar genetics 
Plastid inheritance : variegation in plants
Male sterility in plants
Chloroplast genetics Non-chromosomal genes in Chlamydomonas
Mitochondrial genetics
Paternal inheritance of cpDNA and mtDNA

Types of male sterility. Male sterility in plants can be controlled by nuclear genes or cytoplasm or by both. Therefore, broadly there are atleast three different mechanisms for control of male sterility in plants. These three types would be briefly discussed in this section.
  1. Genetic male sterility. In this type, male sterility is controlled by a single gene and is recessive to fertility, so that the F1individuals would be fertile. In the F2 generation, the fertile and sterile individuals will segregate in 3 : 1 ratio (Fig. 18.12).
  2. Cytoplasmic male sterility. In several crops like maize, cytoplasmic control of male sterility is known. In such cases if female parent is male sterile, F1 progeny would always be male sterile (Fig. 18.13), because cytoplasm is mainly derived from egg obtained from male sterile female parent.
  3. Cytoplasmic-genetic male sterility. In certain other cases, although male sterility is wholly controlled by cytoplasm, but a restorer gene if present in the nucleus will restore fertility. For instance, if female parent is male sterile, then genotype (nucleus) of male parent will determine the phenotype of F1 progeny. The male sterile female parent will have the recessive genotype (rr) with respect to restorer gene. If male parent is RR, F1 progeny would be fertile (Rr). On the other hand, if male parent is rr, the progeny would be male sterile. If F1 individual (Rr)is testcrossed, 50% fertile and 50% male sterile progeny would be obtained (Fig. 18.14).
Inheritance of genetic male sterility in plants.
Fig. 18.12. Inheritance of genetic male sterility in plants.

Maternal inheritance of cytoplasmic male sterility in plants.
Fig. 18.13. Maternal inheritance of cytoplasmic male sterility in plants.
Inheritance of cytoplasmic male sterility and restoration of fertility due to restorer gene.
Fig. 18.14. Inheritance of cytoplasmic male sterility and restoration of fertility due to restorer gene.

During 1990-92, transgenic male sterile and fertility restorer plants have also been produced in Brassica napus, by transfer of 'barnase' and 'barstar' genes from Bacillus amyloliquefaciens (for more details consult Genetic Engineering and Biotechnology 4.  Gene Transfer Methods and Transgenic Organisms).

Cytoplasmic male sterility in maize. Rhoades in 1933, reported the analysis of first cytoplasmic male sterile plants in maize and demonstrated that male sterility was contributed by female parent and that nuclear genes had no influence. This was shown by crossing male sterile plants with wide range of fertile males and by observing that in subsequent generations all progenies were male sterile.

In maize, three male sterile sources (cms) are known, which are called T, C and S. The normal male fertile cytoplasm is called N cytoplasm. Each of the three cms cytoplasms exhibits strict maternal inheritance and even when all chromosomes were replaced by a male fertile source through backcrosses, male sterility could not be overcome (Fig. 18.15). These cytoplasms were a great asset in production of hybrid corn seed at commercial scale. It was also shown that T (Texas) cytoplasm was associated with (i) susceptibility to two diseases, namely southern corn leaf blight disease (Bipolaris maydis race T, formerly known as Helminthosporium maydis)and yellow leaf blight (Phyllstica maydis); (ii) an unusual mitochondrial gene T-urfl3, which encodes a 13 kilodalton polypeptide (URF13). An interaction between fungal toxins and URF3 accounts for specific susceptibility to the above two fungal pathogens. Due to such an association with diseases, use of T cytoplasm in hybrid seed production was greatly curtailed.
Reciprocal crosses between male sterile and male fertile plants (using rare pollen from male sterile). Figure shows a number of back crosses of male sterile as female parent, substituting the nucleus from male fertile. Note that the substitution of male fertile nucleus does not restore fertility in male sterile.
Fig. 18.15. Reciprocal crosses between male sterile and male fertile plants (using rare pollen from male sterile). Figure shows a number of back crosses of male sterile as female parent, substituting the nucleus from male fertile. Note that the substitution of male fertile nucleus does not restore fertility in male sterile.

(a) Role of mitochondria. Recent studies have proved that factors responsible for cytoplasmic male sterility are located in mitochondrial DNA (mtDNA). Six kinds of evidences proved mitochondrial role.

  1. When mitochondrial, DNA was studied in three male sterile cytoplasms (T, C and S) and normal male fertile (N) cytoplasm, it was found that mt DNAs differed in four cytoplasms. It is also apparent that mtDNA from a particular cms (cytoplasmic male sterile) source is stable and conserved. For instance Texas (T) cytoplasm, even after 20 generations of backcrosses had same mtDNA from different T sources. However, when chloroplast DNA (ctDNA) was similarly studied, very little, if any differences were found between ct DNA from four different sources (N, T, C, S). Such an observation was used as an evidence to suggest that cytoplasmic male sterility in higher plants may be associated with mt DNA.
  2. Association of mtDNA has also been shown with disease susceptibility, which itself is associated with cytoplasmic male sterility (cms). Both pathogens, one causing leaf blight disease and the other causing yellow leaf blight are known to produce host specific toxins. These toxins affect the mitochondria of T cytoplasm, but not of N cytoplasm. Such an effect of toxins on mitochondria was observed both inside the cell (in vivo systems) and in cell free mitochondrial preparations (in vitro systems).
  3. The reaction of toxins on mitochondria was modified in cytoplasmic male steriles, which were restored to fertility with the help of restorer genes (Rf1, Rf2-nuclear genes; if these genes are present, male sterile cytoplasm does not express itself). This suggests that restorer genes help restore fertility through' their action on mitochondria.
  4. When T-cytoplasm cells in culture were treated with toxin and resistant cells were selected, then mitochondria of these resistant cells were unaffected by toxin. Mature plants derived from these resistant cells selected originally from male sterile plants, were fertile and disease resistant. It could be shown that this change involved changes in mitochondria only.
  5. It has been shown in several organisms that there are several proteins synthesized under the control of mtDNA and these proteins include cytochrome oxidase, cytochrome b and ATPase. There are evidences available that in T cytoplasm, cytochrome oxidase, cytochrome b and ATPase get affected. Cytoplasm specific proteins characteristic of individual cytoplasms have been shown to be present in N, T, C and S cytoplasms, although the sites of action or function of these distinguishing proteins are not known.
  6. When microsporogenesis was studied in anthers of T and N cytoplasms, mitochondrial degeneration was observed in tapetum and middle layers of anther at the tetrad stage in T cytoplasm and not in N cytoplasm. This degeneration includes, swelling of mitochondria, loss of cristae and internal disorganization. Contrary to this, plastids and other organelles were not affected.
(b) Role of plasmid like DNA in S-cytoplasm. Cytoplasmic male sterility due to S-cytoplasm has been shown to be different from T cytoplasm in several ways. The mtDNA preparations from S-cytoplasm were found to contain two unique plasmid (plasmids are DNA fragments resembling viral DNA molecule; Plasmids, IS Elements, Transposons and Retroelements) like DNAs called SI (6397 bp) and S2 (5453 bp). These plasmid like DNAs could not be isolated from DNA preparations from chloroplasts or nuclei, showing that these are characteristic of mitochondria. Further, the plasmid like DNAs are not found in N (fertile), T (sterile) and C (sterile) cytoplasms, but were present in S-cytoplasm with a variety of nuclear backgrounds, suggesting that these plasmid like DNAs may be responsible for causing male sterility associated with S-cytoplasm.

T and C sterile cytoplasms have been found to be stable, never giving rise to fertile cytoplasms even by applying mutagens. However, S-cytoplasm was found to give rise to fertile condition in some cases due to one of the two kinds of changes : (i) cytoplasmic mutation from male sterile to male fertile or (ii) nuclear mutation giving rise to a new restorer gene. Both these changes could be involved, as shown from experiments when these fertiles derived from S-cytoplasm were crossed as males with cms-S testers. In some cases the progeny was male sterile, suggesting the absence of restorer gene, while in other cases the progeny was semifertile suggesting the presence of restorer gene. In the latter case, restorer was found to be different from the normal nuclear restorer gene Rf3 meant for S-cytoplasm. These new restorers could be located on different chromosomes, which led to the belief that a fertility element having characteristics of an episome (see Plasmids, IS Elements, Transposons and Retroelements) may be present, which gets attached to different chromosomes at different times leading to change from sterile to fertile condition. These fertility elements may actually be the plasmid like DNAs.

It has also been suggested that male fertility genes could be originally located on organellar DNA and were later transposed to a nuclear site giving rise to restorer gene. When this fertility gene is absent both from nucleus and organelle, this might have led to cytoplasmic male sterility. Such a hypothesis for origin of cytoplasmic male sterility is being examined now.