Self-incompatibility in plants
Seiji Takayama & Akira Isogai
Ann. Rev. Plant Biol. (2005) 56: 467-489
Gametophytic self-incompatibility
inhibits pollen tube growth using
different mechanisms
Noni 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 selfincompatibility are encoded by
the S-loci of different plant
species
GAMETOPHYTIC
(GSI)
SPOROPHYTIC
(SSI)
outcome of the interaction between
the pollen tube and the style is
determined by the genotype of the
pollen (gamete)
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
after completion of meiosis
S-locus products are synthesized
before completion of meiosis
growth of the pollen tube arrests in
the style
growth of the pollen tube arrests at
the surface of the stigma
Apocynaceae
Rubiaceae
Convolvulaceae
Solanaceae
ASTERIDS
Scrophularaceae
Bignoniaceae
Oleaceae
Campanulaceae
Asteraceae
GAMETOPHYTIC
SPOROPHYTIC
MIXED
Ericaceae
Sasifragaceae
Geraniaceae
Malvaceae
Brassicaceae
ROSIDS
Fabaceae
Rosaceae
Begoniaceae
Betulaceae
Fagaceae
Papaveraceae
papaveraceae: GSI;
brassicaceae: SSI,
♀-determinant induces a
calcium-dependent
signaling network;
♂-determinant is not yet
identified
♂-determinant is a pollen
ligand; ♀-determinant is a
receptor kinase
solanaceae: GSI;
♀-determinant is a
ribonuclease,
♂-determinant is an
F-box protein
www.ogrod.uj.edu.pl
brassicaceae: SSI,
♂-determinant is a pollen
ligand; ♀-determinant is a
receptor kinase
•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 Slocus 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
www.ogrod.uj.edu.pl
•MLPK (M-locus protein kinase): positive
mediator of SI signaling, loss of function leads to
self-compatibility
SP11/SCR induces
incompatible reactions in
stigma papilla cells
S6S6 stigmas (A) and S2S2 stigmas (B)
were treated with purified recombinant
SCR6 and pollinated with S13 pollen
treatment of stigma
with “self”
SP11/SCR protein
induces signaling
reactions in the
pistil
these signaling
reactions lead to
changes within the
pistil that prevent
growth of “cross”
pollen
Kachroo et al. 2001 Science 293:1824-1826
“solanaceae-TYPE”
Scrophulariaceae
Rosaceae
solanaceae: GSI;
♀-determinant is a
ribonuclease,
♂-determinant is an
F-box protein
the ribonuclease selectively degrades rRNA from
pollen of the matching S-haplotype
a single origin of
S-RNase
mediated
gametophytic
selfincompatibility in
eudicots?
Steinbachs & Holsinger 2002 Mol. Biol. Evol 19: 825-829
Apocynaceae
Rubiaceae
Convolvulaceae
Solanaceae
ASTERIDS
Scrophularaceae
Bignoniaceae
Oleaceae
Campanulaceae
Asteraceae
GAMETOPHYTIC
SPOROPHYTIC
MIXED
Ericaceae
Sasifragaceae
Geraniaceae
Malvaceae
Brassicaceae
ROSIDS
Fabaceae
Rosaceae
Begoniaceae
Betulaceae
Fagaceae
Papaveraceae
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
Golz et al .1999
inhibitor model: all S-RNases
are taken up by the pollen tube,
but S-RNases of non-matching
S-haplotypes are
inhibited/degraded
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;
•instigmatic
S-proteins isolated through
vitro assays of pollen tube inhibition
•bethea receptor
male determinant is believed to
located at the pollen
plasma membrane
•specifically
SBP (S protein binding protein)
binds S-proteins, but
without haplotype specificity
•stigma
interaction of self-pollen with the
induces a calcium-dependent
signaling cascade leading to
programmed cell death in the pollen
(Thomas & Franklin-Tong 2004)
♀-determinant induces a
calcium-dependent
signaling network;
♂-determinant is not yet
identified
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
Summary
G or S?
signaling?
direction
location
of
action
brassicaceae
S
kinase-mediated
♂ to ♀
♀
solanaceae
G
NO
papaveraceae
G
calcium-dependent
♂
♀ to ♂
♂