Segregating population
VIII. Cytoplasmic Resistance
All the resistance genes described until now are inherited in a Mendelian way. They are localized on the chromosomes in the nucleus. However, there are a few exceptions to the Mendelian inheritance of resistance genes. These resistances are inherited via the nonnuclear, cytoplasmic component of the cell. They are encoded by chloroplast or mitochondrial genomes and are transmitted through the mother plant via the female gamete. There is one famous example for cytoplasmic disease resistance in maize (Pring and Lonsdale, 1989). In 1969 and 1970, particular races of the two fungal diseases southern com leaf blight (Cochliobolus heterostrophus or Helminthosporium maydis) and yellow com leaf blight (Mycosphaerella zeae-maydis) caused high losses in maize production. The losses were very high in hybrid varieties which contained the T (Texas) source of cytoplasmic male sterility which was used for an efficient production of hybrid seed. About 17% of the US maize crop was destroyed in 1970.
The susceptibility to the disease was inherited maternally and was later found to be
due to a mutation in the mitochondrially encoded gene T-urf13. In male fertile and disease resistant lines, the T -urf13 gene product is truncated by a frame-shift mutation or deletions. However, when the gene is in a form where it encodes a 13 kD protein, this protein confers sensitivity to the toxins produced by southern com leaf blight and yellow com leaf blight. At that time many lines had the same cytoplasm and this genetic uniformity of the maize lines in terms of susceptibilty to the pathogen resulted in high losses. The experience of the Texas T cytoplasm and its consequences led to a better awareness of the problem of genetic uniformity and its negative impacts. It is now recognized that the use of genetically diverse material is an essential strategy to prevent such epidemics and the value of conserving genetic resources is widely accepted.
In addition, the strategies for the use of these valuable resources of resistance are also much debated. The use of monogenic resistances as a single source of resistance is considered to be very problematic as it risks wasting valuable genetic resources.
Maternal inheritance occurs for traits encoded in the chloroplast or mitochondrial genomes. However, there is also the possibility for paternal effects on inheritance of pathogen resistance. In the common morning glory (ipomoea purpurea), the genetic variance of resistance to anthracnose (caused by Colletotrichum dematium) was found to be largely determined by a paternal effect (Simms and Triplett, 1996). The molecular basis of this paternal inheritance is not known.
IX. Genetic Resources for Resistance
Due to the increasing demands on agricultural resources through an increasing world population the putative sources of resistance have become even more valuable material for plant breeding. In conventional resistance breeding, the major source of resistant germplasm comes from the gene pool of the crop plant itself. Resistances can be found in lines from other breeding programs in the same or in different geographic areas and can be crossed into lines with the desired genetic background. Gene banks containing many different plant accessions, collected from various geographic regions, can also be a very valuable resource for resistant germplasm. There are many examples of resistances which were found in cultivars in different parts of the world. A famous example is the durable leaf rust resistance which is present in the South American wheat variety "Frontana" described above. As wheat is not an endogenous plant in South America, this resistance must have either appeared spontaneously or it was possibly imported from Europe or North America in the form of a land race. Landraces in general are very important sources of genetic variability for resistance breeding and usually consist of mixtures of various genotypes. The conservation of the genetic diversity present in this genetic material is one of the most important tasks not only for plant breeders but for society in general.
An interesting case of a resistance that can be selected from the same cultivar is found in sorghum. There, the resistance to the Milo disease (caused by Periconia circinata) occurs spontaneously in 1 in 8000 plants. An additional source of resistance is represented in the so called "primary gene pool". Thus, close relatives of a crop plant belonging to a different cultivated species, but which can be freely crossed with
146 B. Keller, C. Feuillet & M Messmer
the cultivated plant, form this gene pool. The hexaploid wheat (Triticum aestivum) and spelt (Triticum spelta, an old hexaploid plant similar to wheat which is mainly grown in middle Europe) are other examples of this type of relationship. Additional examples are found among diploid progenitors of polyploid crop plants. E.g., Triticum monococcum, a close relative to the donor of the A-genome of, wheat or T. tauschii, donor of the D-genome can be used as sources for resistance breeding in wheat (Fig. 16).
Figure 16. Wild relatives of crop plants as donors for resistance genes. Wild germplasm contains valuable genetic material for resistance breeding. Three wild grasses are shown. From all of them a number of rust resistance genes have been introgressed into the cultivated wheat by techniques such as embryo rescue and irradiation.
A last and increasingly important class of genetic resources for resistance breeding is found in the wild relatives of crop plants. The genus Lycopersicon comprises wild relatives of the cultivated tomato. Several of the wild relatives have been used as donors of important resistance genes for tomato: L. hirsutum, L. peruvianum and L. pimpinellifolium were the donors of fungal resistance, L. chinese and L. peruvianum for virus resistance and L. peruvianum also for nematode resistance. As most of the genomes of these wild plants recombine more or less freely with the genome of the cultivated tomato, the introgression of the resistance genes was not too difficult.
This is also true for barley, where the wild relative H. spontaneum crosses very well
with the cultivated barley H. vulgare and was a donor for powdery mildew and rust resistance genes. The diversity of resistance genes and physiological reaction types in H. spontaneum seems to be much broader than in cultivated barley. Besides these wild relatives which can be crossed with the cultivated species, there are also wild relatives of crop plants that can only be used as donors of resistant germplasm if cytogenetic manipulations such as irradiation and embryo rescue are used. Examples for such donor plants are relatives of wheat which belong to the wild grasses (Table 3, Fig. 16).
The introgression ofresistance genes from such species normally results in introgressions of large chromosomal segments as it was found in the introgression of the Lr24 leaf rust resistance gene from Agropyron elongatum into wheat (Fig. 17, Schachermayr et aI., 1995). In this case, more than half of the long arm of chromosome 3D was found to be replaced by Agropyron DNA. Such large chromosomal introgressions usually carry a large number of genes and many of the alleles are inferior to the alleles in an adapted, commercially useful variety of a crop plant. Sometimes the genetic background of a line can compensate for these negative traits but the way to adapt the background for this purpose is time-consuming. The molecular isolation of the resistance gene out of the wild plant and subsequent transformation of the single gene into adapted germplasm would allow an efficient use of resistant germplasm without these side effects.
A schematic representation of the advantages of such methods is shown in Fig. 18. In fact, only genetic transformation will allow the efficient use of such wild germplasm in many different breeding programs. The classical techniques are too slow and too cumbersome to use these resistance genes in adapted varieties. Therefore, a lot of the variation of resistances present in wild germplasm is currently not used due to technical limitations.
Table 3. Wild grasses as donors for rust and eyespot disease resistance in the hexaploid wheat (incomplete list, McIntosh et al., 1995).
Donor
Triticum ventricosum
Agropyron elongatum
Triticum umbellulatum
Triticum speltoides
Triticum comosum
Triticum timopheevii
Gene
Lr37, Pch, Yr17, Sr38.
Lr24, Lr19, Lr29, Sr24, Sr26,
Lr9
Lr35, Sr32
Sr34, Yr8
Sr36
Disease
Leaf rust, eye spot (Pseudocercosporella herpotrichoides), yellow rust, stripe rust
Leaf rust, stem rust
Leaf rust
Leaf rust, stem rust
Stem rust, stripe rust
Stem rust
148
80
60
40
20
o
20
40
60
80
100
120 eM
B. Keller, C. Feuillet & M Messmer