Editing Self-incompatibility (section)

==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 (genetics)|locus]] termed '''S''', which has many different [[allele]]s in the [[species]] population. Despite their similar morphological and genetic manifestations, these mechanisms have evolved independently, and are based on different cellular components;<ref name="charlesworth">{{cite journal | vauthors = Charlesworth D, Vekemans X, Castric V, Glémin S | title = Plant self-incompatibility systems: a molecular evolutionary perspective | journal = The New Phytologist | volume = 168 | issue = 1 | pages = 61–69 | date = October 2005 | pmid = 16159321 | doi = 10.1111/j.1469-8137.2005.01443.x |doi-access=free | bibcode = 2005NewPh.168...61C }}</ref> therefore, each mechanism has its own, unique S-[[gene]]s.

The S-locus contains two basic protein [[coding region]]s – one expressed in the [[pistil]], and the other in the [[anther]] and/or pollen (referred to as the '''female''' and '''male determinants''', respectively). Due to their physical proximity, these are genetically [[genetic linkage|linked]], and are inherited as a unit. The units are called S-[[haplotype]]s.  The [[translation (biology)|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. {{cn|date=July 2024}}

Following is a detailed description of the different known mechanisms of SI in plants. {{cn|date=July 2024}}

===Gametophytic self-incompatibility (GSI)===
In '''gametophytic self-incompatibility (GSI)''', the SI [[phenotype]] of the pollen is determined by its own [[gametophyte|gametophytic]] [[ploidy|haploid]] genotype. This is the most common type of SI.<ref name="franklin">{{cite book |doi=10.1016/S0074-7696(08)62485-7 | vauthors = Franklin FC, Lawrence MJ, Franklin-Tong VE |author3-link= Vernonica Franklin-Tong|title=Cell and Molecular Biology of Self-Incompatibility in Flowering Plants |journal=[[Int. Rev. Cytol.]] |volume=158 |pages=1–64 |year=1995 |series=International Review of Cytology |isbn=978-0-12-364561-6 }}</ref> Two different mechanisms of GSI have been described in detail at the molecular level, and their description follows. {{cn|date=July 2024}}

====The RNase-based SI mechanism====
In this mechanism, pollen tube elongation is halted when it has proceeded approximately one third of the way through the [[carpel|style]].<ref name="franklin-tong2003">{{cite journal | vauthors = Franklin-Tong VE, Franklin FC | title = The different mechanisms of gametophytic self-incompatibility | journal = Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences | volume = 358 | issue = 1434 | pages = 1025–1032 | date = June 2003 | pmid = 12831468 | pmc = 1693207 | doi = 10.1098/rstb.2003.1287 | name-list-style = amp }}</ref> The female component [[ribonuclease]] protein, termed '''S-RNase'''<ref name="mcclure">{{cite journal | vauthors = McClure BA, Haring V, Ebert PR, Anderson MA, Simpson RJ, Sakiyama F, Clarke AE | title = Style self-incompatibility gene products of Nicotiana alata are ribonucleases | journal = Nature | volume = 342 | issue = 6252 | pages = 955–957 | year = 1989 | pmid = 2594090 | doi = 10.1038/342955a0 | s2cid = 4321558 | doi-access =  | bibcode = 1989Natur.342..955M }}</ref> probably causes degradation of the [[ribosome|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.<ref name="franklin-tong2003"/>

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<ref name="igic2001">{{cite journal | vauthors = Igic B, Kohn JR | title = Evolutionary relationships among self-incompatibility RNases | journal = Proceedings of the National Academy of Sciences of the United States of America | volume = 98 | issue = 23 | pages = 13167–13171 | date = November 2001 | pmid = 11698683 | pmc = 60842 | doi = 10.1073/pnas.231386798 | name-list-style = amp | doi-access = free }}</ref> and the finding of shared male determinants ('''F-box proteins''')<ref name="qiao2004b">{{cite journal | vauthors = Qiao H, Wang F, Zhao L, Zhou J, Lai Z, Zhang Y, Robbins TP, Xue Y | display-authors = 6 | title = The F-box protein AhSLF-S2 controls the pollen function of S-RNase-based self-incompatibility | journal = The Plant Cell | volume = 16 | issue = 9 | pages = 2307–2322 | date = September 2004 | pmid = 15308757 | pmc = 520935 | doi = 10.1105/tpc.104.024919 | bibcode = 2004PlanC..16.2307Q }}</ref><ref name="ushijima">{{cite journal | vauthors = Ushijima K, Yamane H, Watari A, Kakehi E, Ikeda K, Hauck NR, Iezzoni AF, Tao R | display-authors = 6 | title = The S haplotype-specific F-box protein gene, SFB, is defective in self-compatible haplotypes of Prunus avium and P. mume | journal = The Plant Journal | volume = 39 | issue = 4 | pages = 573–586 | date = August 2004 | pmid = 15272875 | doi = 10.1111/j.1365-313X.2004.02154.x | doi-access = free }}</ref><ref name="sijacic">{{cite journal | vauthors = Sijacic P, Wang X, Skirpan AL, Wang Y, Dowd PE, McCubbin AG, Huang S, Kao TH | display-authors = 6 | title = Identification of the pollen determinant of S-RNase-mediated self-incompatibility | journal = Nature | volume = 429 | issue = 6989 | pages = 302–305 | date = May 2004 | pmid = 15152253 | doi = 10.1038/nature02523 | s2cid = 4427123 | bibcode = 2004Natur.429..302S }}</ref> strongly supported [[Homology (biology)|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.<ref name="igic2001"/><ref name="steinbachs2002">{{cite journal | vauthors = Steinbachs JE, Holsinger KE | title = S-RNase-mediated gametophytic self-incompatibility is ancestral in eudicots | journal = Molecular Biology and Evolution | volume = 19 | issue = 6 | pages = 825–829 | date = June 2002 | pmid = 12032238 | doi = 10.1093/oxfordjournals.molbev.a004139 | name-list-style = amp | doi-access = free }}</ref>

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]],<ref name="asquini2011coffea">{{cite journal | vauthors =Asquini E, Gerdol M, Gasperini D, Igic B, Graziosi G, Pallavicini A |title=S-RNase-like Sequences in Styles of Coffea (Rubiaceae). Evidence for S-RNase Based Gametophytic Self-Incompatibility?|journal=Tropical Plant Biology |volume=4|pages=237–249|year=2011|issue=3–4|doi=10.1007/s12042-011-9085-2|s2cid=11092131}}</ref> [[Rutaceae]],<ref name="liang2020citrus">{{cite journal | vauthors = 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 | display-authors = 6 | title = Evolution of self-compatibility by a mutant S<sub>m</sub>-RNase in citrus | journal = Nature Plants | volume = 6 | issue = 2 | pages = 131–142 | date = February 2020 | pmid = 32055045 | pmc = 7030955 | doi = 10.1038/s41477-020-0597-3 | bibcode = 2020NatPl...6..131L }}</ref> and [[Cactaceae]].<ref name="ramanauskas2021cacti">{{cite journal | vauthors = Ramanauskas K, Igić B | title = RNase-based self-incompatibility in cacti | journal = The New Phytologist | volume = 231 | issue = 5 | pages = 2039–2049 | date = September 2021 | pmid = 34101188 | doi = 10.1111/nph.17541 | name-list-style = amp | s2cid = 235370441 | doi-access = free }}</ref> 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 SI expressed in Prunus species, which functions through self-recognition<ref name="Matsumoto-The-Horticulture-Journal">{{Cite journal |vauthors=Matsumoto D, Tao R |date=2016 |title=Distinct Self-recognition in the Prunus S-RNase-based Gametophytic Self-incompatibility System |url=https://www.jstage.jst.go.jp/article/hortj/85/4/85_MI-IR06/_article |journal=The Horticulture Journal |language=en |volume=85 |issue=4 |pages=289–305 |doi=10.2503/hortj.MI-IR06 |issn=2189-0102 |doi-access=free |access-date=2022-09-28 |archive-date=2022-09-28 |archive-url=https://web.archive.org/web/20220928084909/https://www.jstage.jst.go.jp/article/hortj/85/4/85_MI-IR06/_article |url-status=live }}</ref> (the cytotoxic activity of the S-RNases is inhibited by default and selectively activated by the pollen partner S-haplotype-specific F-box protein (SFB) upon self-pollination), 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.<ref name="franklin-tong2003"/> The mechanism is described in detail for ''[[Papaver rhoeas]]'' and so far appears restricted to the plant family [[Papaveraceae]]. {{cn|date=July 2024}}

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 (biochemistry)|receptor]].<ref name="franklin-tong2003"/> The interaction between male and female determinants transmits a cellular [[signal transduction|signal]] into the pollen tube, resulting in strong influx of [[calcium]] [[cation]]s; this interferes with the intracellular [[concentration]] gradient of calcium [[ion]]s which exists inside the pollen tube, essential for its elongation.<ref>{{cite journal |doi=10.1046/j.1365-313X.1993.04010163.x | vauthors = Franklin-Tong VE, Ride JP, Read ND, Trewavas AJ, Franklin FC |title=The self-incompatibility response in ''Papaver rhoeas'' is mediated by cytosolic free calcium |journal=Plant J. |volume=4 |pages=163–177 |year=1993 |doi-access=free }}</ref><ref>{{cite journal |doi=10.1046/j.1365-313x.1997.12061375.x | vauthors= Franklin-Tong VE, Hackett G, Hepler PK |title=Ratioimaging of Ca21 in the self-incompatibility response in pollen tubes of ''Papaver rhoeas'' |journal=Plant J. |volume=12 |pages=1375–86 |year=1997 |issue=6 |doi-access=free }}</ref><ref>{{cite journal | vauthors = Franklin-Tong VE, Holdaway-Clarke TL, Straatman KR, Kunkel JG, Hepler PK | title = Involvement of extracellular calcium influx in the self-incompatibility response of Papaver rhoeas | journal = The Plant Journal | volume = 29 | issue = 3 | pages = 333–345 | date = February 2002 | pmid = 11844110 | doi = 10.1046/j.1365-313X.2002.01219.x | s2cid = 954229 | doi-access = free }}</ref> 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.<ref name="franklin-tong2003"/>

Subsequently, the [[cytosol]]ic protein '''p26''', a [[pyrophosphatase]], is inhibited by [[phosphorylation]],<ref>{{cite journal | vauthors = Rudd JJ, Franklin F, Lord JM, Franklin-Tong VE | title = Increased Phosphorylation of a 26-kD Pollen Protein Is Induced by the Self-Incompatibility Response in Papaver rhoeas | journal = The Plant Cell | volume = 8 | issue = 4 | pages = 713–724 | date = April 1996 | pmid = 12239397 | pmc = 161131 | doi = 10.1105/tpc.8.4.713 }}</ref> possibly resulting in arrest of [[Biosynthesis|synthesis]] of molecular building blocks, required for tube elongation. There is [[polymerization|depolymerization]] and reorganization of [[actin]] filaments, within the pollen [[cytoskeleton]].<ref>{{cite journal | vauthors = Geitmann A, Snowman BN, Emons AM, Franklin-Tong VE | title = Alterations in the actin cytoskeleton of pollen tubes are induced by the self-incompatibility reaction in Papaver rhoeas | journal = The Plant Cell | volume = 12 | issue = 7 | pages = 1239–1251 | date = July 2000 | pmid = 10899987 | pmc = 149062 | doi = 10.1105/tpc.12.7.1239 | bibcode = 2000PlanC..12.1239G }}</ref><ref>{{cite journal | vauthors = Snowman BN, Kovar DR, Shevchenko G, Franklin-Tong VE, Staiger CJ | title = Signal-mediated depolymerization of actin in pollen during the self-incompatibility response | journal = The Plant Cell | volume = 14 | issue = 10 | pages = 2613–2626 | date = October 2002 | pmid = 12368508 | pmc = 151239 | doi = 10.1105/tpc.002998 | bibcode = 2002PlanC..14.2613S }}</ref> 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,<ref>{{cite journal | vauthors = Jordan ND, Franklin FC, Franklin-Tong VE | title = Evidence for DNA fragmentation triggered in the self-incompatibility response in pollen of Papaver rhoeas | journal = The Plant Journal | volume = 23 | issue = 4 | pages = 471–479 | date = August 2000 | pmid = 10972873 | doi = 10.1046/j.1365-313x.2000.00811.x | doi-access = free }}</ref> and finally (at 10–14 hours), the cell dies [[apoptosis|apoptotically]].<ref name="franklin-tong2003"/><ref>{{cite journal | vauthors = Thomas SG, Franklin-Tong VE | title = Self-incompatibility triggers programmed cell death in Papaver pollen | journal = Nature | volume = 429 | issue = 6989 | pages = 305–309 | date = May 2004 | pmid = 15152254 | doi = 10.1038/nature02540 | name-list-style = amp | s2cid = 4376774 | bibcode = 2004Natur.429..305T }}</ref>

===Sporophytic self-incompatibility (SSI)===
In '''sporophytic self-incompatibility (SSI)''', the SI phenotype of the pollen is determined by the [[ploidity|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]].<ref>{{cite journal |doi=10.1038/hdy.1997.177 | vauthors = Goodwillie C |title=The genetic control of self-incompatibility in ''Linanthus parviflorus'' (Polemoniaceae) |journal=Heredity |volume=79 |pages=424–432 |year=1997 |issue=4|doi-access=free }}</ref> Up to this day, only one mechanism of SSI has been described in detail at the molecular level, in ''[[Brassica]]'' (Brassicaceae). {{cn|date=July 2024}}

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 (genetics)|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 [[Zygosity|homozygous]] for a [[recessive]] S allele.<ref name="hiscock">{{cite journal | vauthors = Hiscock SJ, Tabah DA | title = The different mechanisms of sporophytic self-incompatibility | journal = Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences | volume = 358 | issue = 1434 | pages = 1037–1045 | date = June 2003 | pmid = 12831470 | pmc = 1693206 | doi = 10.1098/rstb.2003.1297 | name-list-style = amp }}</ref>

Compared to a population in which all S alleles are [[co-dominance|co-dominant]], the presence of dominance relationships in the population raises the chances of compatible mating between individuals.<ref name="hiscock"/> 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).<ref>{{cite journal | vauthors = Ockendon DJ |title=Distribution of self-incompatibility alleles and breeding structure of open-pollinated cultivars of Brussels sprouts |journal=Heredity |volume=32 |issue=2 |pages=159–171 |year=1974 |doi=10.1038/hdy.1974.84|doi-access=free }}</ref>

====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 (botany)|tapetum]] [[biological tissue|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).<ref>{{cite journal | vauthors = Schopfer CR, Nasrallah ME, Nasrallah JB | title = The male determinant of self-incompatibility in ''Brassica'' | journal = Science | volume = 286 | issue = 5445 | pages = 1697–1700 | date = November 1999 | pmid = 10576728 | doi = 10.1126/science.286.5445.1697 }}</ref><ref>{{cite journal | vauthors = Takayama S, Shiba H, Iwano M, Shimosato H, Che FS, Kai N, Watanabe M, Suzuki G, Hinata K, Isogai A | display-authors = 6 | title = The pollen determinant of self-incompatibility in ''Brassica campestris'' | journal = Proceedings of the National Academy of Sciences of the United States of America | volume = 97 | issue = 4 | pages = 1920–1925 | date = February 2000 | pmid = 10677556 | pmc = 26537 | doi = 10.1073/pnas.040556397 | doi-access = free | bibcode = 2000PNAS...97.1920T }}</ref> There are possibly up to 100 polymorphs of the S-haplotype in ''Brassica'', and within these there is a dominance hierarchy. {{cn|date=July 2024}}

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.<ref>{{cite journal | vauthors = Stein JC, Howlett B, Boyes DC, Nasrallah ME, Nasrallah JB | title = Molecular cloning of a putative receptor protein kinase gene encoded at the self-incompatibility locus of ''Brassica oleracea'' | journal = Proceedings of the National Academy of Sciences of the United States of America | volume = 88 | issue = 19 | pages = 8816–8820 | date = October 1991 | pmid = 1681543 | pmc = 52601 | doi = 10.1073/pnas.88.19.8816 | doi-access = free | bibcode = 1991PNAS...88.8816S }}: .</ref><ref>{{cite journal | vauthors= Nasrallah JB, Nasrallah ME |title=Pollen–stigma signalling in the sporophytic self-incompatibility response |journal=Plant Cell |volume=5 |issue=10  |pages=1325–35 |year=1993 |doi=10.2307/3869785|jstor=3869785  |bibcode=1993PlanC...5.1325N }}</ref> 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 (biology)|sequence]] to the SRK protein, and seems to function as a [[co-receptor]] for the male determinant, amplifying the SI response.<ref>{{cite journal | vauthors = Takasaki T, Hatakeyama K, Suzuki G, Watanabe M, Isogai A, Hinata K | title = The S receptor kinase determines self-incompatibility in ''Brassica'' stigma | journal = Nature | volume = 403 | issue = 6772 | pages = 913–916 | date = February 2000 | pmid = 10706292 | doi = 10.1038/35002628 | s2cid = 4361474 | bibcode = 2000Natur.403..913T }}</ref>

The interaction between the SRK and SCR/SP11 proteins results in [[autophosphorylation]] of the intracellular kinase domain of SRK,<ref>{{cite journal | vauthors = Schopfer CR, Nasrallah JB | title = Self-incompatibility. Prospects for a novel putative peptide-signaling molecule | journal = Plant Physiology | volume = 124 | issue = 3 | pages = 935–940 | date = November 2000 | pmid = 11080271 | pmc = 1539289 | doi = 10.1104/pp.124.3.935 | name-list-style = amp }}</ref><ref>{{cite journal | vauthors = Takayama S, Shimosato H, Shiba H, Funato M, Che FS, Watanabe M, Iwano M, Isogai A | display-authors = 6 | title = Direct ligand-receptor complex interaction controls ''Brassica'' self-incompatibility | journal = Nature | volume = 413 | issue = 6855 | pages = 534–538 | date = October 2001 | pmid = 11586363 | doi = 10.1038/35097104 | s2cid = 4419954 | bibcode = 2001Natur.413..534T }}</ref> and a signal is transmitted into the [[wikt:papilla|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.<ref>{{cite journal | vauthors = Murase K, Shiba H, Iwano M, Che FS, Watanabe M, Isogai A, Takayama S | title = A membrane-anchored protein kinase involved in ''Brassica'' self-incompatibility signaling | journal = Science | volume = 303 | issue = 5663 | pages = 1516–1519 | date = March 2004 | pmid = 15001779 | doi = 10.1126/science.1093586 | s2cid = 29677122 | bibcode = 2004Sci...303.1516M }}</ref> A downstream signaling cascade leads to proteasomal degradation that produces an SI response.<ref>{{citation |journal = Nature Plants |volume = 1 |issue = 12 |doi=10.1038/nplants.2015.185 |title=Degradation of glyoxalase I in ''Brassica napus'' stigma leads to self-incompatibility response |author=Subramanian Sankaranarayanan, Muhammad Jamshed, and Marcus A. Samuel |date = 2015 |page = 15185 |pmid = 27251720 |bibcode = 2015NatPl...115185S }}</ref>