Self-incompatibility explained

Self-incompatibility (SI) is a general name for several genetic mechanisms that prevent self-fertilization in sexually reproducing organisms, and thus encourage outcrossing and allogamy. It is contrasted with separation of sexes among individuals (dioecy), and their various modes of spatial (herkogamy) and temporal (dichogamy) separation.

SI is best-studied and particularly common in flowering plants,[1] although it is present in other groups, including sea squirts and fungi.[2] In plants with SI, when a pollen grain produced in a plant reaches a stigma of the same plant or another plant with a matching allele or genotype, the process of pollen germination, pollen-tube growth, ovule fertilization, or embryo development is inhibited, and consequently no seeds are produced. SI is one of the most important means of preventing inbreeding and promoting the generation of new genotypes in plants and it is considered one of the causes of the spread and success of angiosperms on Earth.

Mechanisms of single-locus self-incompatibility

The best studied mechanisms of SI act by inhibiting the germination of pollen on stigmas, or the elongation of the pollen tube in the styles. These mechanisms are based on protein-protein interactions, and the best-understood mechanisms are controlled by a single locus termed S, which has many different alleles in the species population. Despite their similar morphological and genetic manifestations, these mechanisms have evolved independently, and are based on different cellular components;[3] therefore, each mechanism has its own, unique S-genes.

The S-locus contains two basic protein coding regions – one expressed in the pistil, and the other in the anther and/or pollen (referred to as the female and male determinants, respectively). Because of their physical proximity, these are genetically linked, and are inherited as a unit. The units are called S-haplotypes. The translation products of the two regions of the S-locus are two proteins which, by interacting with one another, lead to the arrest of pollen germination and/or pollen tube elongation, and thereby generate an SI response, preventing fertilization. However, when a female determinant interacts with a male determinant of a different haplotype, no SI is created, and fertilization ensues. This is a simplistic description of the general mechanism of SI, which is more complicated, and in some species the S-haplotype contains more than two protein coding regions.

Following is a detailed description of the different known mechanisms of SI in plants.

Gametophytic self-incompatibility (GSI)

In gametophytic self-incompatibility (GSI), the SI phenotype of the pollen is determined by its own gametophytic haploid genotype. This is the most common type of SI.[4] Two different mechanisms of GSI have been described in detail at the molecular level, and their description follows.

The RNase mechanism

In this mechanism, pollen tube elongation is halted when it has proceeded approximately one third of the way through the style.[5] The female component ribonuclease protein, termed S-RNase[6] probably causes degradation of the ribosomal RNA (rRNA) inside the pollen tube, in the case of identical male and female S alleles, and consequently pollen tube elongation is arrested, and the pollen grain dies.[5]

Within a decade of the initial confirmation their role in GSI, proteins belonging to the same RNase gene family were also found to cause pollen rejection in species of Rosaceae and Plantaginaceae. Despite initial uncertainty about the common ancestry of RNase-based SI in these distantly related plant families, phylogenetic studies[7] and the finding of shared male determinants (F-box proteins)[8] [9] [10] strongly supported homology across eudicots. Therefore, this mechanism likely arose approximately 90 million years ago, and is the inferred ancestral state for approximately 50% of all plant species.[7] [11]

In the past decade, the predictions about the wide distribution of this mechanism of SI have been confirmed, placing additional support of its single ancient origin. Specifically, a style-expressed T2/S-RNase gene and pollen-expressed F-box genes are now implicated in causing SI among the members of Rubiaceae,[12] Rutaceae,[13] and Cactaceae.[14] Therefore, other mechanisms of SI are thought to be recently derived in eudicots plants, in some cases relatively recently. One particularly interesting case is the Prunus SI systems, which functions through self-recognition[15] (the cytotoxic activity of the S-RNAses is inhibited by default and selectively activated by the pollen partner SFB upon self-pollination), [where "SFB" is a term that stands "for S-haplotype-specific F-box protein", as explained (parenthetically) in the abstract of<ref name="Matsumoto-The-Horticulture-Journal"/>], while SI in the other species with S-RNAse functions through non-self recognition (the S-RNAses are selectively detoxified upon cross-pollination).

The S-glycoprotein mechanism

In this mechanism, pollen growth is inhibited within minutes of its placement on the stigma.[5] The mechanism is described in detail for Papaver rhoeas and so far appears restricted to the plant family Papaveraceae.

The female determinant is a small, extracellular molecule, expressed in the stigma; the identity of the male determinant remains elusive, but it is probably some cell membrane receptor.[5] The interaction between male and female determinants transmits a cellular signal into the pollen tube, resulting in strong influx of calcium cations; this interferes with the intracellular concentration gradient of calcium ions which exists inside the pollen tube, essential for its elongation.[16] [17] [18] The influx of calcium ions arrests tube elongation within 1–2 minutes. At this stage, pollen inhibition is still reversible, and elongation can be resumed by applying certain manipulations, resulting in ovule fertilization.[5]

Subsequently, the cytosolic protein p26, a pyrophosphatase, is inhibited by phosphorylation,[19] possibly resulting in arrest of synthesis of molecular building blocks, required for tube elongation. There is depolymerization and reorganization of actin filaments, within the pollen cytoskeleton.[20] [21] Within 10 minutes from the placement on the stigma, the pollen is committed to a process which ends in its death. At 3–4 hours past pollination, fragmentation of pollen DNA begins,[22] and finally (at 10–14 hours), the cell dies apoptotically.[5] [23]

Sporophytic self-incompatibility (SSI)

In sporophytic self-incompatibility (SSI), the SI phenotype of the pollen is determined by the diploid genotype of the anther (the sporophyte) in which it was created. This form of SI was identified in the families: Brassicaceae, Asteraceae, Convolvulaceae, Betulaceae, Caryophyllaceae, Sterculiaceae and Polemoniaceae.[24] Up to this day, only one mechanism of SSI has been described in detail at the molecular level, in Brassica (Brassicaceae).

Since SSI is determined by a diploid genotype, the pollen and pistil each express the translation products of two different alleles, i.e. two male and two female determinants. Dominance relationships often exist between pairs of alleles, resulting in complicated patterns of compatibility/self-incompatibility. These dominance relationships also allow the generation of individuals homozygous for a recessive S allele.[25]

Compared to a population in which all S alleles are co-dominant, the presence of dominance relationships in the population, raises the chances of compatible mating between individuals.[25] The frequency ratio between recessive and dominant S alleles, reflects a dynamic balance between reproductive assurance (favoured by recessive alleles) and avoidance of selfing (favoured by dominant alleles).[26]

The SI mechanism in Brassica

As previously mentioned, the SI phenotype of the pollen is determined by the diploid genotype of the anther. In Brassica, the pollen coat, derived from the anther's tapetum tissue, carries the translation products of the two S alleles. These are small, cysteine-rich proteins. The male determinant is termed SCR or SP11, and is expressed in the anther tapetum as well as in the microspore and pollen (i.e. sporophytically).[27] [28] There are possibly up to 100 polymorphs of the S-haplotype in Brassica, and within these there is a dominance hierarchy.

The female determinant of the SI response in Brassica, is a transmembrane protein termed SRK, which has an intracellular kinase domain, and a variable extracellular domain.[29] [30] SRK is expressed in the stigma, and probably functions as a receptor for the SCR/SP11 protein in the pollen coat. Another stigmatic protein, termed SLG, is highly similar in sequence to the SRK protein, and seems to function as a co-receptor for the male determinant, amplifying the SI response.[31]

The interaction between the SRK and SCR/SP11 proteins results in autophosphorylation of the intracellular kinase domain of SRK,[32] [33] and a signal is transmitted into the papilla cell of the stigma. Another protein essential for the SI response is MLPK, a serine-threonine kinase, which is anchored to the plasma membrane from its intracellular side.[34] A downstream signaling cascade leads to proteasomal degradation that produces an SI response.

Other mechanisms of self-incompatibility

These mechanisms have received only limited attention in scientific research. Therefore, they are still poorly understood.

2-locus gametophytic self-incompatibility

The grass subfamily Pooideae, and perhaps all of the family Poaceae, have a gametophytic self-incompatibility system that involves two unlinked loci referred to as S and Z.[35] If the alleles expressed at these two loci in the pollen grain both match the corresponding alleles in the pistil, the pollen grain will be recognized as incompatible.[35] At both loci, S and Z, two male and one female determinant can be found. All four male determinants encode proteins belonging to the same family (DUF247) and are predicted to be membrane-bound. The two female determinants are predicted to be secreted proteins with no protein family membership.[36] [37] [38]

Heteromorphic self-incompatibility

A distinct SI mechanism exists in heterostylous flowers, termed heteromorphic self-incompatibility. This mechanism is probably not evolutionarily related to the more familiar mechanisms, which are differentially defined as homomorphic self-incompatibility.[39]

Almost all heterostylous taxa feature SI to some extent. The loci responsible for SI in heterostylous flowers, are strongly linked to the loci responsible for flower polymorphism, and these traits are inherited together. Distyly is determined by a single locus, which has two alleles; tristyly is determined by two loci, each with two alleles. Heteromorphic SI is sporophytic, i.e. both alleles in the male plant, determine the SI response in the pollen. SI loci always contain only two alleles in the population, one of which is dominant over the other, in both pollen and pistil. Variance in SI alleles parallels the variance in flower morphs, thus pollen from one morph can fertilize only pistils from the other morph. In tristylous flowers, each flower contains two types of stamens; each stamen produces pollen capable of fertilizing only one flower morph, out of the three existing morphs.[39]

A population of a distylous plant contains only two SI genotypes: ss and Ss. Fertilization is possible only between genotypes; each genotype cannot fertilize itself.[39] This restriction maintains a 1:1 ratio between the two genotypes in the population; genotypes are usually randomly scattered in space.[40] [41] Tristylous plants contain, in addition to the S locus, the M locus, also with two alleles.[39] The number of possible genotypes is greater here, but a 1:1 ratio exists between individuals of each SI type.[42]

Cryptic self-incompatibility (CSI)

Cryptic self-incompatibility (CSI) exists in a limited number of taxa (for example, there is evidence for CSI in Silene vulgaris, Caryophyllaceae[43]). In this mechanism, the simultaneous presence of cross and self pollen on the same stigma, results in higher seed set from cross pollen, relative to self pollen.[44] However, as opposed to 'complete' or 'absolute' SI, in CSI, self-pollination without the presence of competing cross pollen, results in successive fertilization and seed set;[44] in this way, reproduction is assured, even in the absence of cross-pollination. CSI acts, at least in some species, at the stage of pollen tube elongation, and leads to faster elongation of cross pollen tubes, relative to self pollen tubes. The cellular and molecular mechanisms of CSI have not been described.

The strength of a CSI response can be defined, as the ratio of crossed to selfed ovules, formed when equal amounts of cross and self pollen, are placed upon the stigma; in the taxa described up to this day, this ratio ranges between 3.2 and 11.5.[45]

Late-acting self-incompatibility (LSI)

Late-acting self-incompatibility (LSI) is also termed ovarian self-incompatibility (OSI). In this mechanism, self pollen germinates and reaches the ovules, but no fruit is set.[46] [47] LSI can be pre-zygotic (e.g. deterioration of the embryo sac prior to pollen tube entry, as in Narcissus triandrus[48]) or post-zygotic (malformation of the zygote or embryo, as in certain species of Asclepias and in Spathodea campanulata[49] [50] [51] [52]).

The existence of the LSI mechanism among different taxa and in general, is subject for scientific debate. Criticizers claim, that absence of fruit set is due to genetic defects (homozygosity for lethal recessive alleles), which are the direct result of self-fertilization (inbreeding depression).[53] [54] [55] Supporters, on the other hand, argue for the existence of several basic criteria, which differentiate certain cases of LSI from the inbreeding depression phenomenon.[46] [51]

Self-compatibility (SC)

Self-compatibility (SC) is the absence of genetic mechanisms which prevent self-fertilization resulting in plants that can reproduce successfully via both self-pollen and pollen from other individuals. Approximately one half of angiosperm species are SI, the remainder being SC. Mutations that disable SI (resulting in SC) may become common or entirely dominate in natural populations. Pollinator decline, variability in pollinator service, the so-called "automatic advantage" of self-fertilisation, among other factors, may favor the loss of SI.

Many cultivated plants are SC, although there are notable exceptions, such as apples and Brassica oleracea. Human-mediated artificial selection through selective breeding is often responsible for SC among these agricultural crops. SC enables more efficient breeding techniques to be employed for crop improvement. However, when genetically similar SI cultivars are bred, inbreeding depression can cause a cross-incompatible form of SC to arise, such as in apricots and almonds.[56] [57] In this rare, intraspecific, cross-incompatible mechanism, individuals have more reproductive success when self-pollinated rather than when cross-pollinated with other individuals of the same species. In wild populations, intraspecific cross-incompatibility has been observed in Nothoscordum bivalve.[58]

Further reading

External links

Notes and References

  1. Igic B, Lande R, Kohn JR . Loss of Self-Incompatibility and Its Evolutionary Consequences . International Journal of Plant Sciences . 169. 1 . 93–104 . 2008 . 10.1086/523362 . 15933118 .
  2. Sawada H, Morita M, Iwano M . Self/non-self recognition mechanisms in sexual reproduction: new insight into the self-incompatibility system shared by flowering plants and hermaphroditic animals . Biochemical and Biophysical Research Communications . 450 . 3 . 1142–1148 . August 2014 . 24878524 . 10.1016/j.bbrc.2014.05.099 .
  3. Charlesworth D, Vekemans X, Castric V, Glémin S . Plant self-incompatibility systems: a molecular evolutionary perspective . The New Phytologist . 168 . 1 . 61–69 . October 2005 . 16159321 . 10.1111/j.1469-8137.2005.01443.x . free .
  4. 10.1016/S0074-7696(08)62485-7 . Franklin FC, Lawrence MJ, Franklin-Tong VE . Vernonica Franklin-Tong. Cell and molecular biology of self-incompatibility in flowering plants . . 158 . 1–64 . 1995 . International Review of Cytology . 978-0-12-364561-6 .
  5. Franklin-Tong VE, Franklin FC . The different mechanisms of gametophytic self-incompatibility . Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences . 358 . 1434 . 1025–1032 . June 2003 . 12831468 . 1693207 . 10.1098/rstb.2003.1287 . amp .
  6. McClure BA, Haring V, Ebert PR, Anderson MA, Simpson RJ, Sakiyama F, Clarke AE . Style self-incompatibility gene products of Nicotiana alata are ribonucleases . Nature . 342 . 6252 . 955–957 . 1989 . 2594090 . 10.1038/342955a0 . 4321558 . 1989Natur.342..955M .
  7. Igic B, Kohn JR . Evolutionary relationships among self-incompatibility RNases . Proceedings of the National Academy of Sciences of the United States of America . 98 . 23 . 13167–13171 . November 2001 . 11698683 . 60842 . 10.1073/pnas.231386798 . amp . free .
  8. Qiao H, Wang F, Zhao L, Zhou J, Lai Z, Zhang Y, Robbins TP, Xue Y . 6 . The F-box protein AhSLF-S2 controls the pollen function of S-RNase-based self-incompatibility . The Plant Cell . 16 . 9 . 2307–2322 . September 2004 . 15308757 . 520935 . 10.1105/tpc.104.024919 .
  9. Ushijima K, Yamane H, Watari A, Kakehi E, Ikeda K, Hauck NR, Iezzoni AF, Tao R . 6 . The S haplotype-specific F-box protein gene, SFB, is defective in self-compatible haplotypes of Prunus avium and P. mume . The Plant Journal . 39 . 4 . 573–586 . August 2004 . 15272875 . 10.1111/j.1365-313X.2004.02154.x . free .
  10. Sijacic P, Wang X, Skirpan AL, Wang Y, Dowd PE, McCubbin AG, Huang S, Kao TH . 6 . Identification of the pollen determinant of S-RNase-mediated self-incompatibility . Nature . 429 . 6989 . 302–305 . May 2004 . 15152253 . 10.1038/nature02523 . 4427123 . 2004Natur.429..302S .
  11. Steinbachs JE, Holsinger KE . S-RNase-mediated gametophytic self-incompatibility is ancestral in eudicots . Molecular Biology and Evolution . 19 . 6 . 825–829 . June 2002 . 12032238 . 10.1093/oxfordjournals.molbev.a004139 . amp . free .
  12. Asquini E, Gerdol M, Gasperini D, Igic B, Graziosi G, Pallavicini A . S-RNase-like Sequences in Styles of Coffea (Rubiaceae). Evidence for S-RNase Based Gametophytic Self-Incompatibility?. Tropical Plant Biology . 4. 237–249. 2011. 3–4. 10.1007/s12042-011-9085-2. 11092131.
  13. Liang M, Cao Z, Zhu A, Liu Y, Tao M, Yang H, Xu Q, Wang S, Liu J, Li Y, Chen C, Xie Z, Deng C, Ye J, Guo W, Xu Q, Xia R, Larkin RM, Deng X, Bosch M, Franklin-Tong VE, Chai L . 6 . Evolution of self-compatibility by a mutant Sm-RNase in citrus . Nature Plants . 6 . 2 . 131–142 . February 2020 . 32055045 . 7030955 . 10.1038/s41477-020-0597-3 . 2020NatPl...6..131L .
  14. Ramanauskas K, Igić B . RNase-based self-incompatibility in cacti . The New Phytologist . 231 . 5 . 2039–2049 . September 2021 . 34101188 . 10.1111/nph.17541 . amp . 235370441 . free .
  15. Matsumoto D, Tao R . 2016 . Distinct Self-recognition in the Prunus S-RNase-based Gametophytic Self-incompatibility System . The Horticulture Journal . en . 85 . 4 . 289–305 . 10.2503/hortj.MI-IR06 . 2189-0102 . free . 2022-09-28 . 2022-09-28 . https://web.archive.org/web/20220928084909/https://www.jstage.jst.go.jp/article/hortj/85/4/85_MI-IR06/_article . live .
  16. 10.1046/j.1365-313X.1993.04010163.x . Franklin-Tong VE, Ride JP, Read ND, Trewavas AJ, Franklin FC . The self-incompatibility response in Papaver rhoeas is mediated by cytosolic free calcium . Plant J. . 4 . 163–177 . 1993 . free .
  17. 10.1046/j.1365-313x.1997.12061375.x . Franklin-Tong VE, Hackett G, Hepler PK . Ratioimaging of Ca21 in the self-incompatibility response in pollen tubes of Papaver rhoeas . Plant J. . 12 . 1375–86 . 1997 . 6 . free .
  18. Franklin-Tong VE, Holdaway-Clarke TL, Straatman KR, Kunkel JG, Hepler PK . Involvement of extracellular calcium influx in the self-incompatibility response of Papaver rhoeas . The Plant Journal . 29 . 3 . 333–345 . February 2002 . 11844110 . 10.1046/j.1365-313X.2002.01219.x . 954229 . free .
  19. Rudd JJ, Franklin F, Lord JM, Franklin-Tong VE . Increased Phosphorylation of a 26-kD Pollen Protein Is Induced by the Self-Incompatibility Response in Papaver rhoeas . The Plant Cell . 8 . 4 . 713–724 . April 1996 . 12239397 . 161131 . 10.1105/tpc.8.4.713 .
  20. Geitmann A, Snowman BN, Emons AM, Franklin-Tong VE . Alterations in the actin cytoskeleton of pollen tubes are induced by the self-incompatibility reaction in Papaver rhoeas . The Plant Cell . 12 . 7 . 1239–1251 . July 2000 . 10899987 . 149062 . 10.1105/tpc.12.7.1239 .
  21. Snowman BN, Kovar DR, Shevchenko G, Franklin-Tong VE, Staiger CJ . Signal-mediated depolymerization of actin in pollen during the self-incompatibility response . The Plant Cell . 14 . 10 . 2613–2626 . October 2002 . 12368508 . 151239 . 10.1105/tpc.002998 .
  22. Jordan ND, Franklin FC, Franklin-Tong VE . Evidence for DNA fragmentation triggered in the self-incompatibility response in pollen of Papaver rhoeas . The Plant Journal . 23 . 4 . 471–479 . August 2000 . 10972873 . 10.1046/j.1365-313x.2000.00811.x . free .
  23. Thomas SG, Franklin-Tong VE . Self-incompatibility triggers programmed cell death in Papaver pollen . Nature . 429 . 6989 . 305–309 . May 2004 . 15152254 . 10.1038/nature02540 . amp . 4376774 . 2004Natur.429..305T .
  24. 10.1038/hdy.1997.177 . Goodwillie C . The genetic control of self-incompatibility in Linanthus parviflorus (Polemoniaceae) . Heredity . 79 . 424–432 . 1997 . 4. free .
  25. Hiscock SJ, Tabah DA . The different mechanisms of sporophytic self-incompatibility . Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences . 358 . 1434 . 1037–1045 . June 2003 . 12831470 . 1693206 . 10.1098/rstb.2003.1297 . amp .
  26. Ockendon DJ . Distribution of self-incompatibility alleles and breeding structure of open-pollinated cultivars of Brussels sprouts . Heredity . 32 . 2 . 159–171 . 1974 . 10.1038/hdy.1974.84. free .
  27. Schopfer CR, Nasrallah ME, Nasrallah JB . The male determinant of self-incompatibility in Brassica . Science . 286 . 5445 . 1697–1700 . November 1999 . 10576728 . 10.1126/science.286.5445.1697 .
  28. Takayama S, Shiba H, Iwano M, Shimosato H, Che FS, Kai N, Watanabe M, Suzuki G, Hinata K, Isogai A . 6 . The pollen determinant of self-incompatibility in Brassica campestris . Proceedings of the National Academy of Sciences of the United States of America . 97 . 4 . 1920–1925 . February 2000 . 10677556 . 26537 . 10.1073/pnas.040556397 . free . 2000PNAS...97.1920T .
  29. Stein JC, Howlett B, Boyes DC, Nasrallah ME, Nasrallah JB . Molecular cloning of a putative receptor protein kinase gene encoded at the self-incompatibility locus of Brassica oleracea . Proceedings of the National Academy of Sciences of the United States of America . 88 . 19 . 8816–8820 . October 1991 . 1681543 . 52601 . 10.1073/pnas.88.19.8816 . free . 1991PNAS...88.8816S .

    .

  30. Nasrallah JB, Nasrallah ME . Pollen–stigma signalling in the sporophytic self-incompatibility response . Plant Cell . 5 . 10 . 1325–35 . 1993 . 10.2307/3869785. 3869785 .
  31. Takasaki T, Hatakeyama K, Suzuki G, Watanabe M, Isogai A, Hinata K . The S receptor kinase determines self-incompatibility in Brassica stigma . Nature . 403 . 6772 . 913–916 . February 2000 . 10706292 . 10.1038/35002628 . 4361474 . 2000Natur.403..913T .
  32. Schopfer CR, Nasrallah JB . Self-incompatibility. Prospects for a novel putative peptide-signaling molecule . Plant Physiology . 124 . 3 . 935–940 . November 2000 . 11080271 . 1539289 . 10.1104/pp.124.3.935 . amp .
  33. Takayama S, Shimosato H, Shiba H, Funato M, Che FS, Watanabe M, Iwano M, Isogai A . 6 . Direct ligand-receptor complex interaction controls Brassica self-incompatibility . Nature . 413 . 6855 . 534–538 . October 2001 . 11586363 . 10.1038/35097104 . 4419954 . 2001Natur.413..534T .
  34. Murase K, Shiba H, Iwano M, Che FS, Watanabe M, Isogai A, Takayama S . A membrane-anchored protein kinase involved in Brassica self-incompatibility signaling . Science . 303 . 5663 . 1516–1519 . March 2004 . 15001779 . 10.1126/science.1093586 . 29677122 . 2004Sci...303.1516M .
  35. Baumann U, Juttner J, Bian X, Langridge P . 2000. Self-incompatibility in the Grasses. Annals of Botany. 85. Supplement A. 203–209. 10.1006/anbo.1999.1056. free.
  36. Rohner M, Manzanares C, Yates S, Thorogood D, Copetti D, Lübberstedt T, Asp T, Studer B . 6 . Fine-Mapping and Comparative Genomic Analysis Reveal the Gene Composition at the S and Z Self-incompatibility Loci in Grasses . Molecular Biology and Evolution . 40 . 1 . January 2023 . 36477354 . 9825253 . 10.1093/molbev/msac259 .
  37. Lian X, Zhang S, Huang G, Huang L, Zhang J, Hu F . Confirmation of a Gametophytic Self-Incompatibility in Oryza longistaminata . Frontiers in Plant Science . 12 . 576340 . 2021 . 33868321 . 8044821 . 10.3389/fpls.2021.576340 . free .
  38. Shinozuka H, Cogan NO, Smith KF, Spangenberg GC, Forster JW . Fine-scale comparative genetic and physical mapping supports map-based cloning strategies for the self-incompatibility loci of perennial ryegrass (Lolium perenne L.) . Plant Molecular Biology . 72 . 3 . 343–355 . February 2010 . 19943086 . 10.1007/s11103-009-9574-y . 25404140 .
  39. Ganders FR . The biology of heterostyly . New Zealand Journal of Botany . 17 . 4 . 607–635 . 1979 . 10.1080/0028825x.1979.10432574. free . 1979NZJB...17..607G .
  40. Ornduff R, Weller SG . Pattern diversity of incompatibility groups in Jepsonia heterandra (Saxifragaceae) (SAXIFRAGACEAE) . Evolution; International Journal of Organic Evolution . 29 . 2 . 373–375 . June 1975 . 28555865 . 10.2307/2407228 . 2407228 .
  41. 10.1139/b76-271 . Ganders FR . Pollen flow in distylous populations of Amsinckia (Boraginaceae) . Canadian Journal of Botany . 54 . 2530–5 . 1976 . 22 .
  42. Spieth PT . A necessary condition for equilibrium in systems exhibiting self-incompatible mating . Theoretical Population Biology . 2 . 4 . 404–418 . December 1971 . 5170719 . 10.1016/0040-5809(71)90029-3 . 1971TPBio...2..404S .
  43. Glaettli, M. (2004). Mechanisms involved in the maintenance of inbreeding depression in gynodioecious Silene vulgaris (Caryophyllaceae): an experimental investigation. PhD dissertation, University of Lausanne.
  44. 10.1038/hdy.1956.22 . Bateman AJ . Cryptic self-incompatibility in the wallflower: Cheiranthus cheiri L . Heredity . 10 . 257–261 . 1956 . 2. free .
  45. Travers SE, Mazer SJ . The absence of cryptic self-incompatibility in Clarkia unguiculata (Onagraceae) . American Journal of Botany . 87 . 2 . 191–196 . February 2000 . 10675305 . 10.2307/2656905 . amp . 2656905 .
  46. 10.1007/BF02861001 . Seavey SF, Bawa KS . Late-acting self-incompatibility in angiosperms . Botanical Review . 52 . 195–218 . 1986 . 2 . 1986BotRv..52..195S . 34443387 .
  47. Book: Sage TL, Bertin RI, Williams EG . Ovarian and other late-acting self-incompatibility systems . Williams EG, Knox RB, Clarke AE . Genetic control of self-incompatibility and reproductive development in flowering plants . Advances in Cellular and Molecular Biology of Plants . 1994 . 2 . 116–140 . 10.1007/978-94-017-1669-7_7 . Kluwer Academic . Amsterdam . 978-90-481-4340-5 .
  48. Sage TL, Strumas F, Cole WW, Barrett SC . Differential ovule development following self- and cross-pollination: the basis of self-sterility in Narcissus triandrus (Amaryllidaceae) . American Journal of Botany . 86 . 6 . 855–870 . June 1999 . 10371727 . 10.2307/2656706 . 25585101 . free . 2656706 .
  49. Sage TL, Williams EG . Self-incompatibility in Asclepias . Plant Cell Incomp. Newsl. . 23 . 55–57 . 1991 .
  50. Sparrow FK, Pearson NL . Pollen compatibility in Asclepias syriaca . J. Agric. Res. . 77 . 187–199 . 1948 .
  51. Lipow SR, Wyatt R . Single gene control of postzygotic self-incompatibility in poke milkweed, Asclepias exaltata L . Genetics . 154 . 2 . 893–907 . February 2000 . 10655239 . 1460952 . 10.1093/genetics/154.2.893 . amp .
  52. Bittencourt NS, Gibbs PE, Semir J . Histological study of post-pollination events in Spathodea campanulata beauv. (Bignoniaceae), a species with late-acting self-incompatibility . Annals of Botany . 91 . 7 . 827–834 . June 2003 . 12730069 . 4242391 . 10.1093/aob/mcg088 .
  53. Book: Klekowski EJ . 1988 . Mutation, Developmental Selection, and Plant Evolution. . Columbia University Press . New York .
  54. 10.2307/2444892 . Waser NM, Price MV . Reproductive costs of self-pollination in Ipomopsis aggregata (Polemoniaceae): are ovules usurped? . 2444892 . American Journal of Botany . 78 . 8 . 1036–43 . 1991 .
  55. Book: Lughadha N . Owen SJ, Rudall PJ . Preferential outcrossing in Gomidesia (Myrtaceae) is maintained by a post-zygotic mechanism. . Reproductive biology in systematics, conservation and economic botany . London . Royal Botanic Gardens, Kew . 1998 . 363–379 . 10.13140/RG.2.1.2787.0247 .
  56. Egea J, Burgos L . Detecting cross-incompatibility of three North American apricot cultivars and establishing the first incompatibility group in apricot . Journal of the American Society for Horticultural Science . November 1996 . 121 . 6 . 1002–1005 . 10.21273/JASHS.121.6.1002 . 25 December 2020. free .
  57. Gómez EM, Dicenta F, Batlle I, Romero A, Ortega E . Cross-incompatibility in the cultivated almond (Prunus dulcis): Updating, revision and correction . Scientia Horticulturae . 19 February 2019 . 245 . 218–223 . 10.1016/j.scienta.2018.09.054 . 2019ScHor.245..218G . 25 December 2020 . 20.500.12327/55 . 92428859 . free . 19 March 2022 . https://web.archive.org/web/20220319083847/https://www.sciencedirect.com/science/article/abs/pii/S0304423818306642 . live .
  58. Weiherer DS, Eckardt K, Bernhardt P . Comparative floral ecology and breeding systems between sympatric populations of Nothoscordum bivalve and Allium stellatum (Amaryllidaceae) . Journal of Pollination Ecology . July 2020 . 26 . 3 . 16–31 . 10.26786/1920-7603(2020)585 . 225237548 . 25 December 2020 . free . 29 July 2024 . https://web.archive.org/web/20240729180617/https://pollinationecology.org/index.php/jpe . live .

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