Self incompatibility in plants

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Under self-incompatibility in plants refers to strategies of seed plants , after pollination , the fertilization by their own pollen ( autogamy ) or to prevent genetically similar pollen. In the case of self-fertilization , it can statistically more often happen that previously hidden ( heterozygous recessive ) negative characteristics are expressed and the offspring are disadvantaged as a result. This is why there are systems in the flowers of some plants that can recognize related or own pollen and thus prevent fertilization by them.

The systems of self-incompatibility ( SI for short ) are roughly differentiated according to the location of the recognition reaction. If this takes place on the basis of features of the tube-like germinating pollen interior ( pollen tube ), one speaks of gametophytic self-incompatibility (GSI). In contrast to this, recognition is based on characteristics of the pollen surface ( deposited by the paternal sporophyte ). If the individuals of the sporophytic SI that can be crossed with one another, ie the individuals that are not "related" to one another, differ in certain morphological features, this is called heteromorphic self-incompatibility (HMSI). If, on the other hand, all individuals have the same appearance, then (homomorphic) sporophytic self-incompatibility (SSI) is present. There is also a combination of gametophytic and sporophytic self-incompatibility (GSSI). The disadvantage of one's own or closely related pollen in pollen germination is a possible way that can prevent self-fertilization, one speaks of cryptic self-incompatibility (CSI).

In addition, there are other mechanisms, e.g. B. prevent the formation of offspring from self-fertilization , for example via genes that lead to the death of embryonic tissue ( lethal alleles ) and other modes of action, even after fertilization. Its classification as a "self-incompatibility system" is controversial among botanists , since self-fertilization does take place, but ultimately no offspring are produced from it.

Botanical and genetic principles

Plants form two generations. One generation, called the “ gametophyte ”, has only one set of chromosomes , which is also known as “ haploid ”. The gametophyte now forms sex cells, so-called “ gametes ”: male and female. These merge to form a zygote , a process known as " fertilization ". The zygote now has a double set of chromosomes (" diploid ") and forms the next generation. This is called the “ sporophyte ” and it is also what one generally sees as a “seed plant”, that is to say as a tree or “flower”. The gametophyte is reduced to very few cells in seed plants. The female gametophyte is located in the ovule , in the ovary is, the male gametophyte inside of the pollen. After pollination, the haploid pollen interior germinates in the form of a tube (hence also called “pollen tube”) and fertilizes the also haploid “egg cell” in the ovule. This creates a new diploid sporophyte.

In principle, fertilization works in the same way in plants as it does in animals: two simple sets of chromosomes become double. The advantage of a double set of chromosomes is that defective genes can be compensated for by the corresponding genes on the second chromosome. This is also one of the reasons why most more highly developed living things are not haploid. However, if a diploid organism with a defective gene fertilizes itself, it is possible that the two defective gene versions collide. This means that compensation is no longer possible and that can mean disadvantages or even death. Self-fertilization can therefore have negative consequences and is therefore often prevented in general.

In order to prevent self-pollination in seed plants, one can try to rule out self-pollination . This is implemented quite often, but mostly not particularly effective. Another method would be to recognize your “own” pollen and keep it from fertilizing. This requires three things: characteristics of the pollen , characteristics of the scar and a mechanism for preventing or stopping pollen that is recognized as undesirable from growing. Since genetics were not yet fully understood at the beginning of research into self-incompatibility systems , it was assumed that this occurs through a single gene. This was called the "S-gene" , whereby the S stands for "self-incompatibility". Nowadays, however, it is known that only a few very closely spaced (“ linked ”) genes are responsible for this. Correctly, one should therefore speak of an “S gene locus ”. Since every plant has such S-gene loci, the genes must exist in different forms (so-called “ alleles ”) in order to ensure a distinction between “self” and “foreign”. This is very similar to an ID card: everyone has one, but each one looks a little different. These different alleles result in proteins with mostly small but important differences that are necessary for (self) recognition. Depending on the system, the number of alleles is 2 (HMSI) or fluctuates between 20 and 70 (GSI and SSI).

In order to ensure real “self-recognition”, the respective allele for the pollen characteristic and the allele for the matching scar feature must always be available coupled. If they did not do this, the self-recognition traits would be distributed independently of one another within a group ( population ) of plants over time ( see also Mendel's 3rd rule ). This is due to the fact that the formation of haploid germ cells (more precisely in meiosis ) leads to an exchange of genetic material between the duplicate chromosomes ( recombination ). The closer together the genes for the traits, the less likely it is that they will separate during recombination.

Which characteristics of pollen or stigma are responsible for the detection and how this works exactly depends on the respective SI systems. This also means that they are not necessarily related ( homologous ) to one another in evolutionary terms . However, since they all cause self-sterility, they are still summarized under the umbrella term "S-genes". Due to the distribution of the incompatibility systems within the seed plants , it is assumed that some of them have arisen several times independently of one another and that parallel developments have also taken place within a system.

In the case of the sweet grasses (Poaceae), in addition to the S gene, another gene that functions analogously is known, which is known as the “Z gene”. Both the S-allele and the Z-allele must match for fertilization to be terminated. When sharp buttercup ( Ranunculus acris ) was a third, in which sugar beet ( Beta vulgaris even discovered a fourth gene). However, Mulcahy & Bergamini-Mulcahy pointed out in 1983 that multiple independent self-incompatibility genes make self-recognition less and less likely.

Gametophytic Self Incompatibility (GSI)

In the case of gametophytic self-incompatibility, closely related pollen (father plant with S 1 , S 3 ) can contribute to fertilization up to 50% , namely those with the foreign S allele.

At GSI, the recognition reaction takes place through the genotype of the gametophyte. Since the germinating pollen tube is gametophytic and therefore only has one set of chromosomes ( haploid ), it has only one S allele. In the stylus to be pollinating flower are two alleles, as it sporophytisch is thus diploid. The two alleles are usually expressed there simultaneously (codominance).

The GSI has a certain disadvantage due to the gametophytic detection, which enables fertilization with genetically similar pollen. Z. B. a male parent with S 1 , S 3 with a female parent with S 1 , S 2 , 50% of the pollen (namely the S 3 pollen) can fertilize the egg cell. Since genetic material is exchanged between the chromosomes during meiosis during gametophyte development ( recombination ), identical ( homozygous ) gene areas can occur in both chromosomes in the fertilized egg cell (zygote) . This can lead to negative effects in the case of defective gene copies.

The GSI is often correlated with certain characteristics. When pollinated, the pollen is often still two-seeded. The male gametophyte thus consists of the pollen tube cell and the generative cell, which only later divides into the two sperm cells. The protective layer on the grain surface ( cuticle ) is discontinuous, that has gaps or thin spots. Through this, the scar secretes a sugar-rich liquid ("moist scar"). In grasses , these correlations do not exist, although their self-incompatibility else via the gametophyte. Grass pollen has three nuclei and the surface of the scar is very hairy and otherwise dry.

The GSI is known in 56 plant families . In addition to the rose family , nightshade family and figwort , the sweet grasses are also represented.

In the tobacco species Nicotiana alata , pollen is recognized by the gametophytes.

RNase mechanism

The biochemical functionality has not yet been fully clarified, but it has been found that in many cases ( nightshade family , petunias , rose family ) RNA- degrading enzymes ( RNases ) are formed in the style cells. These migrate into the pollen tube and thus prevent the formation of proteins there. Pollen's own gene products, so-called “S-coupled F-box proteins” ( SFB ), attack all “foreign” RNase versions that are not encoded in their own genome , like an immune system . In doing so, they ignore those stylus RNase versions that are also encoded in the pollen (self-recognition). These “own” RNases then bring the protein biosynthesis of the pollen tube to a standstill. The pollen tube dies in the stylus and the sperm cells do not reach the egg cell. When the pollen tube dies, callose is then deposited in the stylus.

Since the mechanism runs through very similar RNase types and in each case via F-box proteins, it is assumed that this mechanism has arisen once and has been lost again in many groups. By molecular dating of this system is estimated to be about 90 million years ago.

Apoptosis mechanism

In poppy plants , however, the recognized "self" as the S allele triggers by Ca 2+ of ions related signal chain that only the growth of the pollen tube by degradation of the actin - cytoskeleton stops and then programmed cell death ( apoptosis causes) in the pollen tube cell.

(Homomorphic) Sporophytic Self-Incompatibility (SSI)

Regardless of which allele the gametophyte now has, the two alleles of the paternal sporophyte decide at SSI.

In SSI, the recognition reaction does not depend on the gametophyte , but on the pollen-forming sporophyte . As a result, both alleles of the diploid genome of the “father” play a role. This is possible through the detection of proteins in the outer pollen wall layer ( exine ), which was deposited by the "paternal" sporophyte. If only one S allele matches that of the maternal sporophyte to be fertilized, a rejection reaction occurs. In practice, however, it is usually the case with the S-gene of the pollen-forming sporophyte that only one of the two alleles is expressed ( dominance ). As with the GSI, this can lead to partial homozygosity , i.e. directly related genome segments come together, which should actually be prevented.

With SSI, the mostly three-cell pollen is hindered during germination. In contrast to the GSI, the protective layer of the scar ( cuticle ) is continuous, i.e. without gaps and secretes little or no fluid (“dry scar”). In contrast to heteromorphic self-incompatibility, incompatibility between closely related genotypes is not linked to any morphological features.

Homomorphic sporophytic self-incompatibility (SSI) is known in 8 plant families , including the daisy family , the bindweed family and the cruciferous family .

Gametophytic-Sporophytic Self-Incompatibility (GSSI)

In GSSI, the reaction depends on both the sporophytic pollen outer layer ( exine ) and the gametophyte. It therefore represents a combination of GSI and SSI.

In the cabbage ( Brassica ) two linked genes, each with a large number of alleles, were identified. In the receptive region of the scar on the surface thereof is a protein called SRK ( S - r preceptor k deposited INASE). The protein with the name SCR ( s mall, c ystein r ich pollen-coat protein, sometimes also called SP11), which is very close in the genome and therefore only rarely separated by crossing-over , is expressed in pollen. The SCR protein quite often has the amino acid cysteine and is located on the surface of the pollen. Unusually, the two alleles of the SCR gene are not expressed simultaneously (codominant), as known from the SSI, but there are dominant and recessive alleles. The dominant alleles are produced by the tapetum (the tissue of the parent plant that forms the outer layer of the pollen) and in the pollen tube itself, so that sporophytic detection occurs. The recessive SCR gene variants are only expressed in the pollen tube, so that a gametophytic SI then takes place.

It was found in some cruciferous plants ( Brassica , Eruca , Raphanus ) and sunflower plants ( Hypochaeris , Pippau ). Since the examples were found within the “typical SSI families”, a general gametophytic influence on sporophytic self-incompatibility systems cannot be ruled out.

Heteromorphic Sporophytic Self-Incompatibility (HMSI or HSI)

The stemless cowslip ( Primula vulgaris ) in the short-handled morphine ('thrum').

The HMSI describes self-incompatibility coupled with different morphological (= heteromorphic) features. The best known feature is the length of the stylus ( heterostyly ). If there are two forms in which the stamens are above the stylus (Kurzgriffligkeit, English: thrum ) and once the stylus is above the stamens (Langgriffligkeit, English: pin ), one speaks of distyly . A well-known example that Clusius recognized as early as 1583 is the primrose . However, it was only Charles Darwin in 1877 that recognized the connection between uneven grip and self-sterility. Individuals with the same flower structure do not produce offspring. However, there are other features which are correlated with the stylus length, such as the size of the dust bag ( Lungenkraut and others), pen color (eg. B. Eichhornia ) or -behaarung (z. B. sorrel ). Although the different length of the stylus is a visually striking feature, it is not mandatory for the HMSI. The self-sterile beach carnation ( Armeria maritima ) has different morphs , but does not have different styluses and stamens of different lengths, but other morphological features such as e.g. B. different pollen size. However, the occurrence of heterostyly is not necessarily (but very often) associated with self-incompatibility.

There are also trimorphic variants in which the stylus and two stamen circles can be in three versions to each other. A distinction is made depending on whether the stylus is at the bottom, in the middle or at the top. Such Tristylie there are about the Purple Loosestrife , on sorrel plants and the water hyacinth .

The heteromorphic sporophytic self-incompatibility combined with the sporophytic self-recognition a reduction of the self-pollination, in that pollen and stigma are spatially separated ( hercogamy ). Due to the different placement of the pollen at the pollinator, differently shaped morphs are preferentially pollinated, which increases the efficiency of the system.

The pollen reaction is sporophytic, so both gene products of the alleles on the pollen outer layer determine whether the pollen can germinate or not.

Heteromorphies coupled with self-incompatibility are known in about 25 families and 155 genera. They are particularly common in the red family , but also in the lead root family , linseed family and much more.

Genetics of the distyle representatives

The stemless cowslip ( Primula vulgaris ) in the long-handled morphine ('pin').

In HMSI, the S gene in distyle representatives is only ever present in two states (alleles): "S" and "s". The S allele is dominant over the s allele , so it always prevails. Since there are two alleles in the plant, effectively “S” applies to Ss and effectively “s” to ss. The homozygous S-type “SS” is excluded, as it could only arise through the fertilization of Ss with Ss, which is prevented by self-incompatibility. So only SS and SS individuals can cross with each other. This then results in 50% SS and 50% SS individuals. It is often the case that Ss individuals develop short styles and SS individuals develop long styles (e.g. buckwheat , forsythia , primroses ), but less often the other way round ( Hypericum aegypticum ).

The S-gene in the distyled primroses consists of three very closely linked genes. The first gene ( G or g ) is responsible for the stylus length (with the dominant G short style, with g long ones), the nature of the scar papillae (with G larger papillae) and the incompatibility reaction of the scar. Gen 2 ( P or p ) is responsible for the pollen grain size (with P smaller pollen than with p ) and the reaction of the pollen grain, while the third gene ( A or a ) determines the height of the anthers (with A standing tall). Rare new combinations of these characteristics have proven the diversity of the gene loci, i.e. the existence of several individual genes . So you know z. B. also primroses, where the stylus and the anthers are at the same height ("homostyl"). This can be explained if G and a (stylus short and anthers low) or if g and A (stylus long and anthers high) come together.

Genetics of the tristyle representatives

The horned wood sorrel ( Oxalis corniculata ) is tristyle, here in the long stylus morph.

In tristyle species with HMSI, the genetics are a bit more complicated. There are two gene loci (“S” and “M”) with two alleles each (S / s and M / m). The characteristics of M only come to the fore if S is present with the recessive allele, ie as "ss" (one says, S is epistatic over M). If the dominant S-allele occurs, the style is short, regardless of which M-allele occurs. If the dominant S-allele does not occur (only with “ss”), the middle pen is created when a dominant M-allele occurs (with ssMm, ssmM and ssMM). The morph with the long stylus only arises if both genes only carry the recessive alleles (ssmm). This system is often so pronounced among representatives with tristyly, but there are again exceptions.

The pollen of the long stamens is fertile on long pistils, the pollen of medium stamens on medium-long pistils and correspondingly on short ones. Since each flower has 2 stamen circles, one morph can fertilize the other two morphs.

As with the distyle groups, some species have lost their self-incompatibility. B. also self-compatible wood sorrel species with tristyly. The loss of an allele can also result in secondary distyly.

Cryptic Self Incompatibility (CSI)

Under cryptic self-incompatibility (English: cryptic self-incompatibility ) refers to the phenomenon that in an otherwise self-compatible type, the pollen tubes of foreign pollen grow faster than its own. The CSI is not a separate form of self-incompatibility, but only describes that cross-pollination is actively preferred. The cryptic SI was found z. B. in gold lacquer , in Decodon verticillatus or in Campanulastrum americanum

Lethal alleles

Self-fertilization is also prevented in gymnosperms and ferns . However, since these have neither scar nor stylus, it is assumed that there are lethal alleles. These are recessive versions of genes which, if they are duplicated (homozygous) in the diploid chromosome set , lead to the death of the fertilized egg cell or the embryo. This is especially the case when there is self-fertilization. A large number of genes with lethal alleles are usually found in ferns and naked samers. Since the genetics of the lethal allele actually has nothing to do with the other self-incompatibility systems, it is controversial whether one should add them or not. In the case of the lethal alleles, fertilization also takes place, but there are no offspring. The argument that the next generation only depends on whether or not there are also individuals from self-fertilization, on the other hand, would add lethal alleles to the SI systems.

Self-incompatibility with late onset - Postzygotic SI (PSI) - Ovarian SI

These terms summarize phenomena that describe the death of the pollen tube cell shortly before the egg cell or the death of the egg cell that is already self-fertilized. While the late SI probably has a delayed gametophytic SI, it is not clear with the other forms whether it is a real self-incompatibility reaction or whether they describe the expression of negative recessive characteristics in homozygosity ( inbred depression ) ( see also lethal alleles). The disagreement of terms is also justified by the unknown, more precise mechanisms.

Importance for populations

Above all, the loss of self-incompatibility and the associated distyly allowed the ancestor of Linum lewisii to gain a foothold in North America, because the blue-flowering flax species are otherwise common in the ancient world.

If plants can no longer fertilize themselves or close relatives, this also has an impact on the population and the spread of the species .

Self-fertilization clearly has its disadvantages, such as a loss of genetic diversity over time. Due to the recombination during meiosis in the first generation after self-fertilization, many alleles remain in an individual in different versions ( heterozygous ), but after about 8 generations over 99% of the genome is identical in both chromosomes. The probability that there are negative properties among them, which then come into play and reduce the plant's ability to survive, increases steadily. Mating between two siblings delays this effect, but does not prevent it. It must also be borne in mind that a genetic defect can already have strong effects.

On the other hand, the restriction to cross-fertilization ( xenogamy ) also represents a danger. B. reduced to a few individuals by a catastrophic event, it can happen that these are suddenly reproductively isolated and the population collapses completely. The repopulation of distant habitats , such as an island or another mountain, corresponds to such a situation. Usually only one or a few spreading units ( diaspores ) are drifted over long distances or only a few germinate . If the species are themselves incompatible, no permanent repopulation can take place; the population dies out again after a generation. The loss of self-sterility is therefore a prerequisite for spreading to foreign areas. Thus, for example, the immigrant to Europe sorrel TYPES Although tristyl, but capable of self-fertilization. However, the use of non-sexual reproduction ( apomixis ) is also a possibility to enable the colonization of new locations and at the same time to prevent self-fertilization.

Self incompatibility and the ecology of a plant species are therefore closely linked. Self-sterility would certainly be a disadvantage for species that are weak in competition and only rarely flower and / or occur in low densities . Mostly, however, it is the case that having a self-incompatibility system does not categorically rule out self-fertilization. As in almost all characteristics, there is often a variation in the strength of the reaction to self-recognition with self-incompatibility. Thus, the advantages and disadvantages of both reproductive systems are scattered, which enables them to survive even adverse conditions.

Importance in plant breeding

The self-incompatibility presents plant breeders in particular with major problems. Since it is widespread in seed plants , various plants used by humans are of course self-sterile. Important crops such as rice and maize belong to the gametophytically self-incompatible sweet grasses . Economically interesting mutants can therefore not be obtained and propagated by self-pollination. Self-incompatibility also makes breeding difficult for many other species such as tobacco or garden flowers, especially hybrid breeding .

A widely used solution for the maintenance of interesting individuals is vegetative propagation, for example via cuttings . In the course of increasing knowledge of the physiological processes in plants, other techniques, such as the extraction and cultivation of whole plants from divisible tissue ( meristems ), are also possible. With the help of plant hormones, a complete plant can develop from the resulting, still undifferentiated tissue ( callus ) . The desired characteristics of the resulting clones can then u. U. be crossed into existing breeding lines or varieties through various crossing strategies. However, this method is time-consuming and laborious.

In 1955 , Marianne Kroh proposed a method for bypassing self-incompatibility systems by removing the scar and bringing the pollen directly into the pollen tube-conducting stylus tissue . In many cases, this can bypass the rejection reactions, as they mainly take place in the scar. Another but complicated method of forcing self-fertilization is by fusion of protoplasts . For this purpose, specimens with a simple set of chromosomes (" haploid ") are first made from the target plants , cells are removed from them and these are freed from the cell wall . The resulting “naked” artificial germ cells can be B. be combined via cell fusion and treated like a callus ( see above ).

history

With the (re) discovery of gender segregation in plants ( dikline ) in the 18th century, questions about pollination and the role of insects also arose . Many botanists dealt with the topic, including Charles Darwin , who concluded from experimental series in 1877 that cross- pollination was the rule (Knight-Darwin's law) and that there had to be pressure to select the different types of flowers to separate the sexes.

However, it was only in the 20th century that deeper insights could be gained. As early as 1905, through new research after the rediscovery of Mendel's rules, Bateson and Gregory suggested that heterostyly must be encoded by two alleles of a gene. The next breakthrough in research into plant self-incompatibility came only in 1925. Edward M. East and AJ Mangelsdorf discovered in experiments with tobacco that self-incompatibility is controlled by a “gene” that must be present in many alleles. They found out that pollination only takes place if the S allele in the pollen does not match the alleles of the plant to be pollinated, which is now known as gametophytic self-incompatibility (GSI).

In 1950 , a self-incompatibility was discovered in the composites by DU Gerstel in Guayule ( Parthenium argentatum ) and MR Hughes and EB Babcock in Stink-Pippau ( Crepis foetida ), which was not due to just one allele (that of the gametophyte), but two alleles of pollen is determined. From their observations, they concluded that there was a sporophytic SI reaction. In 1956, A. Lundquist and DL Hayman discovered in parallel the existence of a second S gene in sweet grasses, which is called the “Z gene”. The former later discovered other self-incompatibility genes that can be found in a plant. Just one year later, in 1957, JL Brewbaker discovered that there is usually a connection between sporophytic or gametophytic SI and the number of cells in the pollen and the moisture in the stigma.

The biochemical relationships, however, did not begin to be understood until 1974. Above all, the work of Jack Heslop-Harrison and Yolande Heslop-Harrison as well as RB Knox , who recognized proteins of the pollen outer layer (exine) as a factor of self-incompatibility in cruciferous plants , provided significant impetus.

The molecular functions, however, have only been understood since the 1990s, based on the availability of molecular biological methods. In 1947, Dan Lewis suspected a lock-and-key mechanism with regard to separate features of pollen and stigma , but it would only be possible to detect it around 50 years later. Research today (as of 2006) is only at the beginning of understanding the molecular interactions and thus also the real diversity and evolutionary development of the systems.

Individual evidence

  1. ↑ David L. Mulcahy, Gabriella Bergamini-Mulcahy: Gametophytic self-incompatibility reexamined. In: Science . Vol. 230, No. 4603, 1983, pp. 1247-1251, doi : 10.1126 / science.220.4603.1247 .
  2. ↑ Bruce A. McClure, Julie E. Gray, Marilyn A. Anderson, Adrienne E. Clarke: Self-incompatibility in Nicotiana alata involves degradation of pollen rRNA. In: Nature . Vol. 347, 1990, pp. 757-760.
  3. ↑ Paja Sijacic, Xi Wang, Andrea L. Skirpan, Yan Wang, Peter E. Dowd, Andrew G. McCubbin, Shihshieh Huang, Teh-hui Kao: Identification of the pollen determinant of S-RNase-mediated self-incompatibility. In: Nature . Vol. 429, 2004, pp. 302-305.
  4. ↑ Hong Qiao, Fei Wang, Lan Zhao, Junli Zhou, Zhao Lai, Yansheng Zhang, Timothy P. Robbins, Yongbiao Xue: The F-box protein AhSLF-S2 controls the pollen function of S-RNase-based self-incompatibility. In: Plant Cell. Vol. 16, No. 9, 2004, ISSN  1040-4651 , pp. 2307-2322, doi : 10.1105 / tpc.104.024919 .
  5. ↑ Boris Igic, Joshua R. Kohn: Evolutionary relationships among self-incompatibility RNases. In: Proceedings of the National Academy of Sciences of the United States of America . Vol. 98, No. 23, 2001, pp. 13167-13171, doi : 10.1073 / pnas.231386798 .
  6. ↑ Steve Thomas, Kim Osman, Barend HJ de Graaf, Galina Shevchenko, Mike Wheeler, Chris Franklin, Noni Franklin-Tong: Investigating mechanisms involved in the self-incompatibility response in Papaver rhoeas. In: Proceedings of the Royal Society of London B . Vol. 358, No. 1434, 2003, pp. 1033-1036, PMC 1693190 (free full text).
  7. ↑ Deborah Charlesworth, Xavier Vekemans, Vincent Castric, Sylvain Glémin: Plant self-incompatibility systems: a molecular evolutionary perspective. In: New Phytologist. Vol. 168, No. 1, 2005, ISSN  0028-646X , pp. 61-69, PMID 16159321 , doi : 10.1111 / j.1469-8137.2005.01443.x .
  8. ↑ Fred R. Ganders: The biology of heterostyly. In: New Zealand Journal of Botany. Vol. 17, No. 4, 1979, ISSN  0028-825X , pp. 607-635, doi : 10.1080 / 0028825X . 1979.10432574 .
  9. ^ AJ Bateman: Cryptic self-incompatibility in the wallflower: Cheiranthus cheiri L. In: Heredity. Vol. 10, 1956, ISSN  0018-067X , pp. 257-261, ( online ).
  10. ↑ Christopher G. Eckert, Maryl Allen: Cryptic self-incompatibility in tristylous Decodon verticillatus (Lythraceae). In: American Journal of Botany. Vol. 84, No. 10, 1997, ISSN  0002-9122 , pp. 1391-1397, JSTOR 2446137 .
  11. ↑ Leah J. Kruszewski, Laura F. Galloway: Explaining Outcrossing Rate in Campanulastrum americanum (Campanulaceae): Geitonogamy and Cryptic Self-Incompatibility. In: International Journal of Plant Sciences. Vol. 167, No. 3, 2006, pp. 455-461, JSTOR 10.1086 / 501051 .
  12. ↑ Max Hagman: Incompatibility in forest trees. In: Proceedings of the Royal Society of London B . Vol. 188, No. 1092, 1975, pp. 313-326, JSTOR 76332 .
  13. ^ Claire G. Williams, Yi Zhou, Sarah E. Hall: A chromosomal region promoting outcrossing in a conifer. In: Genetics. Vol. 159, No. 3, 2001, pp. 1283-1289, PMC 1461856 (free full text).
  14. ↑ Tammy L. Sage, Robert I. Bertin, Elizabeth G. Williams: Ovarian and other late-acting self-incompatibility systems. In: Elizabeth G. Williams, Adrienne E. Clarke, R. Bruce Knox (eds.): Genetic control of self-incompatibility and reproductive development in flowering plants (= Advances in Cellular and Molecular Biology of Plants. 2). Kluwer Academic Publishing, Dordrecht et al. 1994, ISBN 0-7923-2574-5 , pp. 116-140, doi : 10.1007 / 978-94-017-1669-7_7 .
  15. ↑ Steven R. Seavey, Kamaljit S. Bawa: Late-acting self-incompatibility in angiosperms. In: The Botanical Review. Vol. 52, No. 2, 1986, ISSN  0006-8101 , pp. 195-219, doi : 10.1007 / BF02861001 .
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literature
This article was added to the list of excellent articles on May 20, 2006 in this version .