Self-incompatibility in plantsSeiji Takayama & Akira Isogai

Ann. Rev. Plant Biol. (2005) 56: 467-489

Gametophytic self-incompatibility inhibits pollen tube growth using

different mechanismsNoni Franklin-Tong & F. Chris H. Franklin

TRENDS in Plant Science (2003) 8: 598-605

self-incompatibility

very important in the evolution of flowering plants

~70% of plants are hermaphroditic

SI appears to have evolved

independently at least 21 times SI has also been independently

lost in numerous lineages, due to human or environmental selection

pressures

the S-locus

in dicots, self-incompatibility maps to a single genetic locus(grasses have 2 unlinked loci!)

molecular dissection of the S-locus in several plant species has shown that:

the S-locus consists of multiple, tightly-linked genes, encoding male and female compatibility determinants

divergent mechanisms of self-incompatibility are encoded by the S-loci of different plant species

GAMETOPHYTIC(GSI)

outcome of the interaction between the pollen tube and the style is

determined by the genotype of the pollen (gamete)

S-locus products are synthesized after completion of meiosis

growth of the pollen tube arrests in the style

SPOROPHYTIC(SSI)

outcome of the interaction between the pollen tube and the style is

determined by the genotype of the sporophyte (diploid tissue)

S-locus products are synthesized before completion of meiosis

growth of the pollen tube arrests at the surface of the stigma

Papaveraceae

ASTERIDS

ROSIDSRANUNCULIDAE

MAGNOLID DICOTS

FagaceaeBetulaceae

Begoniaceae

Rosaceae

Fabaceae

Sasifragaceae

Geraniaceae

BrassicaceaeMalvaceae

ApocynaceaeRubiaceae

ConvolvulaceaeSolanaceae

ScrophularaceaeBignoniaceaeOleaceae

CampanulaceaeAsteraceae

Ericaceae

GAMETOPHYTIC

SPOROPHYTIC

MIXED

papaveraceae: GSI; ♀-determinant induces a

calcium-dependent signaling network;

♂-determinant is not yet identified

solanaceae: GSI; ♀-determinant is a

ribonuclease, ♂-determinant is an

F-box protein

brassicaceae: SSI, ♂-determinant is a pollen ligand; ♀-determinant is a receptor kinase

www.ogrod.uj.edu.pl

brassicaceae: SSI, ♂-determinant is a pollen ligand; ♀-determinant is a receptor kinase

www.ogrod.uj.edu.pl

•SLG (S-locus glycoproteins): identified immunologically as an S-haplotype-specific antigen; SLG is not sufficient (or necessary) for SI response, but enhances the activity of SRK

•SRK (S-locus receptor kinase): identified by sequencing S-locus; high similarity to SLG

•SP11/SCR (S-locus protein 11/S-locus cysteine-rich): identified though cloning and sequencing of the S-locus region and polymorphic gene identification using differential display; induces incompatible reactions in stigma papilla cells (SP11/SCR of matching S-locus haplotype induced autophosphorylation of SRK in stigma plasma membrane)

•ARC1 (Armadillo repeat-containing 1): identified through protein interaction with SRK, proposed to promote the degradation of stigmatic proteins promoting pollen germination/growth

•MLPK (M-locus protein kinase): positive mediator of SI signaling, loss of function leads to self-compatibility

these signaling reactions lead to changes within the pistil that prevent growth of “cross” pollen

treatment of stigma with “self” SP11/SCR protein induces signaling reactions in the pistil

SP11/SCR induces incompatible reactions in stigma papilla cells

Kachroo et al. 2001 Science 293:1824-1826

S6S6 stigmas (A) and S2S2 stigmas (B) were treated with purified recombinant SCR6 and pollinated with S13 pollen

solanaceae: GSI; ♀-determinant is a

ribonuclease, ♂-determinant is an

F-box protein

“solanaceae-TYPE”

Scrophulariaceae Rosaceae

the ribonuclease selectively degrades rRNA from pollen of the matching S-haplotype

a single origin of S-RNase mediated

gametophytic self-

incompatibility in eudicots?

Steinbachs & Holsinger 2002 Mol. Biol. Evol 19: 825-829

Papaveraceae

ASTERIDS

ROSIDSRANUNCULIDAE

MAGNOLID DICOTS

FagaceaeBetulaceae

Begoniaceae

Rosaceae

Fabaceae

Sasifragaceae

Geraniaceae

BrassicaceaeMalvaceae

ApocynaceaeRubiaceae

ConvolvulaceaeSolanaceae

ScrophularaceaeBignoniaceaeOleaceae

CampanulaceaeAsteraceae

Ericaceae

GAMETOPHYTIC

SPOROPHYTIC

MIXED

SI system S-RNase mediated

♂-determinant: receptor or inhibitor?

receptor model: whether or not a pollen tube is degraded depends on selective uptake of S-RNases by the pollen tube

inhibitor model: all S-RNases are taken up by the pollen tube, but S-RNases of non-matching S-haplotypes are inhibited/degraded

Golz et al .1999

additional factors:

• HT-B (small, asparagine-rich protein expressed late in stylar development)

• 4936-factor (not yet cloned, mutations result in self-compatibility)

• 120kDa glycoprotein (abundant in style, taken up by growing pollen tubes, interacts with S-RNase in vitro)

in the absence of HT-B or 4936-factor, S-RNase remains compartmentalized in pollen tubes and does not cause pollen

rejection

Goldraij et al. 2006 Nature 439: 805-810

papaveraceae: GSI; ♀-determinant induces a

calcium-dependent signaling network;

♂-determinant is not yet identified

•stigmatic S-proteins isolated through in vitro assays of pollen tube inhibition

•the male determinant is believed to be a receptor located at the pollen plasma membrane

•SBP (S protein binding protein) specifically binds S-proteins, but without haplotype specificity

•interaction of self-pollen with the stigma induces a calcium-dependent signaling cascade leading to programmed cell death in the pollen (Thomas & Franklin-Tong 2004)

Summary

●SI is an important mechanism for preventing inbreeding in plants

●3 different mechanisms of SI have been described at the molecular level●Sporophytic SI dependent on a kinase-mediated

signaling cascade

●Gametophytic SI based on selective degradation of pollen rRNA by S-RNases

●Gametophytic SI based on a calcium-dependent (MAPK) signaling cascade leading to cell death in pollen

brassicaceae

solanaceae

papaveraceae

G or S?

S

G

G

signaling?

kinase-mediated

calcium-dependent

NO

direction

♂ to ♀

♀ to ♂

location of action

♀

♂

♂

Summary