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Plant Physiol, January 2001, Vol. 125, pp. 105-108
Recognizing Self in the Self-Incompatibility Response
Ram
Dixit and
June B.
Nasrallah*
Department of Plant Biology, Cornell University, Ithaca, New York
14853
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INTRODUCTION |
François Jacob once
facetiously lamented the arrangement in the human body whereby
reproduction is the only function for which an individual is
equipped with only one-half of the necessary organs, thus
entailing the expenditure of a substantial amount of time and energy
into finding the other half (10). The spatial separation of the sexual
partners (or organs) is indeed an obligatory feature of sexual
reproduction, but curiously, organisms that are hermaphroditic and
hence have the potential for self-fertilization are frequently seen to
be indulging in the social facet of sexuality, i.e. the search for a mate.
Plants, being sessile organisms, cannot actively search for mates but
have contrived a variety of genetic and nongenetic mechanisms to hinder
self-pollination and promote cross-pollination. The time and energy
spent on facilitating cross-pollination is amply compensated for by an
increased vigor of the organism as demonstrated by Darwin (4).
Self-incompatibility (SI) is an example of a genetic barrier to
self-fertilization and represents the most common antiselfing mechanism
among the angiosperms.
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CLASSICAL VIEW OF THE SI RESPONSE |
The SI response is a phenomenon that occurs after pollination has
taken place and entails the recognition and selective inhibition of
"self" pollen grains by cells of the pistil. Early genetic studies
(for review, see 5) of the Solanaceae and Brassicaceae (crucifer)
families established that specificity in the SI response is controlled
by a single multi-allelic locus called the S locus, and that
the SI response is instigated when pollen and pistil are derived from
plants sharing a common S-locus variant. Subsequent studies
in other taxa established a similar single-locus control in some, but
also demonstrated control by more than one recognition locus in others
(as in the Poaceae family).
Because the ultimate outcome of the SI reaction i.e. inhibition of
self-related pollen and prevention of self-fertilizationis the same
in different plant families, one view proposed SI to be monophyletic in
origin. Yet it was also recognized that dramatic differences occur in
the SI response of different taxa. One difference, which has formed the
basis of a major classification scheme for SI systems, is the mode of
genetic control of the pollen SI phenotype. In sporophytic SI, the
pollen phenotype is determined by the diploid S complement
of the parent plant, whereas in gametophytic SI, the pollen phenotype
is determined by the S-locus variant carried in its haploid
genome. Even more dramatic are differences in the site of inhibition of
pollen or pollen tube. For example, in crucifers, the epidermal cells
of the stigma prevent hydration and further development of the
incompatible pollen grains, whereas in the Solanaceae family,
incompatible pollen tubes are free to make their way into the style
where their growth is severely and selectively retarded. In all
systems, the S locus was thought to encode molecules that
act as S-allele-specific tags on pollen grain or tube and on
cells of the pistil which allow the discrimination of self versus
non-self. One hypothesis regarding the mechanism of self-recognition was that an inhibitory dimer is produced by homophilic binding of
identical SI gene products carried by the pollen and pistil. A second
hypothesis envisioned the S locus to be a complex locus containing distinct pollen and pistil specificity determinants (for
review, see 5).
In this note, we summarize the major progress achieved during the last
2 decades in isolating genes that encode the determinants of
specificity in the SI response and understanding the molecular basis of
self-recognition.
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MOLECULAR DIVERSITY OF SI SYSTEMS |
Starting in the 1980s, molecular methods were applied to the study
of SI in species exhibiting single-locus control, namely Brassica sp., Nicotiana sp. and
other Solanaceous plants, and Papaver rhoeas. Based
on the earlier success of immunochemical methods in identifying an
S-locus-linked stigma-specific protein in
Brassica (17), these molecular studies focused initially on the isolation of genes that were: (a) expressed specifically in the
pistil at the site of pollen arrest and in correlation with the
acquisition of the SI response by the developing pistil, (b) polymorphic between strains carrying different SI specificities, and
(c) genetically linked to the S locus. These studies
resulted in the isolation of the S-locus glycoprotein gene
(16) and later the S-receptor kinase gene (19) in
Brassica (a sporophytic system), the S-RNase gene
(1) in Nicotiana (a gametophytic system), and the
S glycoprotein (9) in Papaver (also a
gametophytic system). It is significant that the
S-locus-associated genes isolated in each of the three
species were found to bear no sequence similarity to one another,
providing a first clue that SI evolved independently and probably
multiple times in different lineages of the angiosperms. Thus, a major
outcome of these studies was the realization that the "S
loci" of the Brassicaceae, Solanaceaeae, and Papaveraceae families
are nonhomologous loci, and that the term "SI" represents not one
process but a variety of mechanistically distinct processes (see below)
that are similar only in their ultimate outcome. In addition, the
uniqueness of the SI system in the three families refutes any
relatedness assumed by the classification of SI systems on the basis of
gametophytic or sporophytic control of pollen SI phenotype.
THE PISTOL (SIC) IS THE LAST LINE OF DEFENSE FOR THE FLOWER
In the Solanaceae family, as well as the Scrophulariaceae and the
Rosaceae families, which also have an S-RNase gene
associated with their S loci, SI is proposed to be based on
the cytotoxic effect of the S-RNase on self-related pollen tubes. In
Nicotiana and Petunia sp., the activity of
the S-RNases has been shown to be necessary for the SI response and
transformation experiments have demonstrated that the S-RNase
represents the pistil component of the SI response (13, 15). The
S-RNase is secreted into the transmitting tissue and is proposed to
enter the pollen tube and degrade its cellular RNA (for review, see 7).
The pollen SI factor in this system is proposed to be an
S-allele-specific transporter or an intracellular
S-allele-specific inhibitor of the S-RNase (7).
In the case of Papaver, the stigma-specific S
glycoprotein is a small protein capable of S-allele-specific
inhibition of pollen tube development in an in vitro pollen germination
assay (12), presumably by interacting with a pollen-derived
S-allele-specific receptor. This interaction would
presumably result in the variety of responses observed within
incompatible pollen tubes upon exposure to S glycoprotein,
including protein phosphorylation, elevation in cytosolic
Ca2+ levels, and changes in the actin
cytoskeleton, all of which are known to result in inhibition of pollen
tube growth (11).
In Brassica, self-recognition is based on the activity of
the S-receptor protein kinase (SRK), which is expressed specifically in
the stigma epidermis. Of the three SI systems investigated so far, the
Brassica system is unique in that the biochemical events
that are precipitated by self-recognition and that result in the
inhibition of self pollen occur in cells of the pistil rather than in
the pollen or pollen tube. The requirement for SRK in SI was known for
some time from the analysis of self-fertile plants that occur
spontaneously or are generated by a transgenic approach. However, it
was only recently that a transgenic approach succeeded at modifying SI
specificity in stigmas (3, 21). These transgenic experiments
demonstrated that SRK is the determinant of SI specificity in the
stigma, and that the cell wall-localized S-locus glycoprotein, which
shares a high degree of sequence similarity with the ectodomain of SRK,
enhances the strength of the SI response (21), possibly by facilitating
post-translational maturation and accumulation of the SRK receptor (6).
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THE POLLEN DETERMINANT OF SPECIFICITY IN THE SI RESPONSE |
In comparison with the pistil, pollen has suffered from a general
lack of understanding through the ages. Before the experimental demonstration of plant sexuality by Camerarius, the involvement of the
ovary in seed production was never in doubt; however, pollen had yet to
be perceived as male sexual structures. Pollen was instead perceived to
represent a type of floral excrement or to function in the service of
bees that deliberately acquired pollen to achieve better stability in
flight. Our understanding of the pollen component of the SI response
has suffered a similar lapse in understanding.
Subsequent to the isolation of the pistil components of SI in
Brassica, the Solanaceae family, and Papaver,
work focused on determining if these genes also functioned in pollen,
as predicted by the dimer hypothesis of S-gene action. When
it became obvious that they did not, a variety of approaches were used
to identify the pollen determinant of SI, including differential
cloning strategies as well as development of bioassays for pollen
proteins (20). It was ultimately direct cloning of the S
locus that resulted in a major breakthrough and the isolation of the
pollen SI specificity gene in Brassica (18). Sequence
analysis and transcriptional mapping of a chromosomal segment spanning
the SLG and SRK genes led to the
identification of SCR (S-locus Cys rich), a
gene that is exclusively expressed in the anthers and exhibits
S-genotype-associated polymorphism. It is most significant
that analysis of a loss-of-function mutant strain and gain-of-function
transgenic plants proved that SCR is both necessary and
sufficient for determining SI specificty in pollen (18). It is expected
that the small (<8 kD) hydrophilic SCR protein is secreted and
incorporated into the pollen coat. Thus, the stigma and pollen SI
specificity molecules of crucifers are located at the surfaces of the
interacting cells as was predicted by Bateman in the 1950s based on the
rapidity of the SI response in this family.
The S-locus-encoded molecules provide specificity for the SI
response, but the culmination of the response, i.e. inhibition of self
pollen, must involve the participation of other proteins. In
Brassica, the current working model for the SI response
envisages that SCR would bind to SRK in an
S-genotype-specific manner. This results in the activation
within the stigma epidermal cell of a signal transduction cascade, the
endpoint(s) of which are the immediate cause of self-pollen arrest (18;
Fig. 1). Details of this SRK-mediated
signal cascade are poorly understood although some elements are
beginning to emerge.
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Figure 1.
Recognition of self pollen in Brassica.
The diagram shows the three genes of the S-locus complex
(introns are not shown for simplicity) and the interactions proposed
for the S-locus-encoded recognition molecules at the
pollen-stigma interface. The genes and the corresponding protein
products are color coded.
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THE S LOCUS AS A COMPLEX MULTIGENIC LOCUS |
A major finding of the molecular analysis of SI in
Brassica, and one that is likely to hold true for SI in
other taxa with single-locus control, has been that the genetic
behavior of the S locus as a simple Mendelian locus masks a
complex and rearranged physical structure. To reflect this complexity,
the "S alleles" of classical SI genetics are now
referred to as "S haplotypes." The Brassica S
haplotyes that have been mapped to date can vary significantly in
overall physical size and in the relative orientations and positioning
of their genes (2, 22). In this, the Brassica S locus is
similar to other recognition loci, such as the mating type loci of
Chlamydamonas reinhardtii and fungi, where structural heteromorphism is known to affect the frequency of recombination and
contribute to the maintenance of recognition genes in a tightly linked
genetic unit.
Another feature shared by plant SI systems and other recognition
systems is the extensive polymorphisms of their genes. S locus genes have attained some of the highest levels of allelic polymorphism known for any locus, consistent with the expectation that
S haplotypes are subject to diversifying selection. This is
especially true for the small SCR protein, allelic forms of which
exhibit strict conservation of only eight Cys residues and one Gly
residue (18, 22). A challenge for the future is to understand how
"matched" allelic polymorphisms in the pistil and pollen
determinants of SI, and thus new SI specificities, are generated.
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THE ROAD AHEAD |
Although substantial progress has been made in the study of SI,
much remains to be done. In the Solanaceae family and
Papaver, the search for the male component is still a topic
of hot pursuit. In Brassica, the identification of the
pollen identity factor (SCR) is sure to cause a spurt of activity
toward deciphering the nature of the SRK-SCR interaction and subsequent
SRK activation. In all three systems, the particular domains or
residues in the S-locus genes that are responsible for the
unique SI specificity of each variant remain to be elucidated, although
some progress on this issue has been made in P. rhoeas (12)
and Solanum sp. (14).
Of great interest, but also more difficult to tackle, are questions
relating to the origin of SI and S-locus genes. It now appears that the SI recognition genes were recruited from genes that
are expressed in a variety of plant organs and presumably perform
functions unrelated to pollination. For example, the Brassica SRK gene is the prototype of a class of receptor-like protein kinases that occurs in dicots and monocots, and SCR is
likely to also be one member of a family of ligands. Functional
analysis of these gene families is obviously critical for understanding the relationship of the SI self-recognition genes with gene sets that
control plant growth and development or regulate the plant's defense
response. Furthermore, with the identification of SCR, the putative
ligand for SRK, the Brassica SRK-SCR system becomes one of
only two receptor-ligand pairs known in plants. The other is CLV1, a
member of the Leu-rich repeat class of receptor-like protein kinases,
members of which function in plant development or defense, and its
putative ligand, the small CLV3 peptide (8). The identification of
these genes promises to usher in a productive era in the study of
peptide signaling in plants, the regulation of receptor activity and
ligand availability, and mechanisms of receptor activation. In this
arena, the natural polymorphism of the Brassica SI genes
should provide a unique resource for investigating the range of changes
that can sustain a productive receptor-ligand interaction and for
understanding the still obscure selection mechanisms that direct the
coevolution of receptor-ligand pairs.
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FOOTNOTES |
*
E-mail jbn2{at}cornell.edu; fax 607-255-5407.
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LITERATURE CITED |
-
Anderson MA, Cornish EC, Mau S-L, Williams EG, Hoggart R, Atkinson A, Bonig I, Greg B, Simpson R, Roche PJ, Haley JD, Penschow JD, Niall HD, Tregear GW, Coghlan JP, Crawford RJ, Clarke AE
(1986)
Nature
321: 38-44
[CrossRef]
-
Boyes DC, Nasrallah ME, Verbalov J, Nasrallah JB
(1997)
Plant Cell
9: 237-247
[Abstract]
-
Cui Y, Bi Y-M, Brugiere N, Arnoldo M, Rothstein SJ
(2000)
Proc Natl Acad Sci USA
97: 3713-3717
[Abstract/Free Full Text]
-
Darwin C
(1876)
The Effects of Cross- and Self-Fertilization in the Vegetable Kingdom. Murray, London
-
de Nettancourt D
(1977)
Incompatibility in Angiosperms. Springer, Berlin
-
Dixit R, Nasrallah ME, Nasrallah JB
(2000)
Plant Physiol
24: 297-311
-
Dodds PN, Clarke AE, Newbigin E
(1996)
Cell
85: 141-144
[CrossRef][Web of Science][Medline]
-
Fletcher JC, Brand U, Running MP, Simon R, Meyerowitz EM
(1999)
Science
283: 1911-1914
[Abstract/Free Full Text]
-
Foote HCC, Ride JP, Franklin-Tong VE, Walker EA, Lawrence MJ, Franklin FCH
(1994)
Proc Natl Acad Sci USA
91: 2265-2269
[Abstract/Free Full Text]
-
Jacob F
(1980)
The Possible and The Actual. University of Washington Press, Seattle
-
Jordan ND, Ride JP, Rudd JJ, Davies EM, Franklin-Tong VE, Franklin FCH
(2000)
Ann Bot
85: 197-202
[Abstract/Free Full Text]
-
Kakeda K, Jordan ND, Conner A, Ride JP, Franklin-Tong VE, Franklin FCH
(1998)
Plant Cell
10: 1723-1731
[Abstract/Free Full Text]
-
Lee HS, Huang SS, Kao TH
(1994)
Nature
367: 560-563
[CrossRef][Medline]
-
Matton DP, Maes O, Laublin G, Xike Q, Bertrand C, Morse D, Cappadocia M
(1997)
Plant Cell
9: 1757-1766
[Abstract]
-
Murfett J, Atherton TL, Mou B, Gasser CS, McClure BA
(1994)
Nature
367: 563-566
[CrossRef][Medline]
-
Nasrallah JB, Kao T-H, Goldberg ML, Nasrallah ME
(1985)
Nature
318: 263-267
[CrossRef]
-
Nasrallah ME, Wallace DH
(1967)
Nature
213: 700-701
-
Schopfer CR, Nasrallah ME, Nasrallah JB
(1999)
Science
286: 1697-1700
[Abstract/Free Full Text]
-
Stein JC, Howlett B, Boyes DC, Nasrallah ME, Nasrallah JB
(1991)
Proc Natl Acad Sci USA
88: 8816-8820
[Abstract/Free Full Text]
-
Stephenson AG, Doughty J, Dixon S, Elleman CJ, Hiscock SJ, Dickinson HG
(1997)
Plant J
12: 1351-1359
[CrossRef][Web of Science]
-
Takasaki T, Hatakeyama K, Suzuki G, Watanabe M, Isogai M, Hinata K
(2000)
Nature
403: 913-916
[CrossRef][Medline]
-
Takayama S, Shiba H, Iwano M, Shimosato H, Che F-S, Kai N, Watanabe M, Suzuki G, Hinata K, Isogai A
(2000)
Proc Natl Acad Sci USA
97: 1920-1925
[Abstract/Free Full Text]
© 2001 American Society of Plant Physiologists
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INTRODUCTION
CLASSICAL VIEW OF THE...