Year: 2002
Type: article
Abstract: Cell–cell interactions in plants are expected to occur between adjoining cells that share a common developmental history. One exception is the interaction of the pollen or pollen tube with cells of the pistil. As a result, pollen–pistil interactions have emerged as models for the study of cell-to-cell signaling, particularly in the context of genetic self-incompatibility (SI). SI is an intraspecific mating barrier found in a large number of species distributed among many plant families that allows cells of the pistil to recognize and reject self-related pollen (De Nettancourt, 2001). Many SI systems are controlled genetically by a single highly polymorphic locus, the S locus, and pollen inhibition occurs when pollen and pistil are derived from plants that express the same S locus variant(s). Molecular studies performed during the last two decades have demonstrated that the term “self-incompatibility” does not represent one mechanism of self-recognition and that the S loci of different families are not homologous. Rather, the term encompasses a collection of disparate systems that have distinct evolutionary histories and are based on mechanistically different strategies for the inhibition of self-related pollen. One strategy used by members of the Solanaceae (McClure et al., 1989), Rosaceae (Sassa et al., 1993), Scrophulariaceae (Xue et al., 1996), and Campanulaceae (Stephenson et al., 2000) is directed at inhibiting pollen tubes after they have grown into the style and is based on the cytotoxic activity of stylar-secreted S-RNases, which act inside the pollen tube to inhibit its growth. Other strategies, such as those used by the Brassicaceae and Papavaraceae, are directed at preventing pollen germination or pollen tube ingress into the pistil; in this strategy, self pollen is inhibited at the stigma surface within minutes of pollen–stigma contact. It is in these two families that SI relies on the perception and transduction of specific signals, albeit using distinct molecular determinants and fundamentally different mechanisms, for the inhibition of self pollen. In the Brassicaceae, a signal is carried by the pollen grain, which is perceived and transduced into a cellular response within the stigma epidermis. In Papaver, the signal is produced by stigmatic cells and perceived by pollen, resulting in a transduction cascade within the pollen tube (Rudd and Franklin-Tong, 2001). Here, we review our understanding of cell-to-cell signaling in the SI system of the Brassicaceae, which is currently the only system for which the stigma and pollen recognition components are known. Scanning Electron Micrograph of Pollination in Brassica Showing the Interaction between a Pollen Grain (Po) and a Stigma Papillar Cell (P). Magnification ×400. The S-Locus Genes of Crucifers, Receptor–Ligand Interactions, and Signal Transduction in the SI Response. (A) Arrangement of SI genes in the Brassica S 8 haplotype and structures of their protein products. Arrows above the genes indicate the 5′→3′ orientations of the genes. The extracellular S domains are shown in red, and the kinase domain of SRK is shown in yellow. White bars in the S domains represent 12 conserved Cys residues, and circles indicate glycosylation sites. Black and gray boxes represent the signal sequences in SRK/SLG and SCR, respectively. The blue box represents the SRK transmembrane domain. (B) A model of signal perception and response in the SI response. Molecules that have been shown conclusively to function in SI are shown as closed shapes. SRK is shown spanning the plasma membrane (orange bar) of the stigmatic epidermal cell, with its kinase (red circle) in the cytoplasm and its ectodomain (red crescent) extending into the cell wall (stippled area). SLG and eSRK are shown as crescents in the papillar cell wall. SCR molecules are shown as dimeric molecules in the papillar cell wall, to which they are transferred from the pollen coat of pollen. “Self” SCR (green circles) interacts with the SRK ectodomain and triggers a signaling cascade, whereas “nonself” SCR (purple triangles) does not. ARC1 is shown by a gray box, with red bars indicating arm repeats and a yellow bar indicating the U box. Phosphorylation is indicated by “P” enclosed by a circle. Less-well-defined associations are indicated by a question mark and patterned shape. Thioredoxins (THX) are shown by stippled turquoise boxes that are associated with the SRK kinase domain only in the absence of ligand, although the mode of its interaction with SRK activation is not understood. An inhibitor of SI (stippled blue polygon) is drawn as a possible target for ubiquitination. The possible involvement of additional SRK substrates is shown by a brown striped half-circle associated with the activated SRK kinase domain. The black arrows and question marks indicate unknown components of the SI signal transduction pathway, which is likely to terminate with the modification of the papillar cell membrane or wall at the site of contact with self pollen. (C) Mutations that lead to loss of the SI response in stigmas. The diagram shows mutations in SRK, ARC1, and SLG and their consequences. eSRK, soluble form of the SRK ectodomain; SCR, S-locus Cys-rich protein; SLG, S-locus glycoprotein; SRK, S-locus receptor protein kinase. The determinant of SI specificity in the stigma epidermis is the S locus receptor protein kinase (SRK) gene. The SRK nucleotide sequence predicts a protein with an extracellular domain, a single-pass transmembrane domain, and a cytoplasmic kinase domain (Figure 2A) (Stein et al., 1991) that exhibits Ser/Thr kinase activity (Goring and Rothstein, 1992; Stein and Nasrallah, 1993). SRK is the prototype of a ubiquitous class of plant receptor-like protein kinases (Shiu and Bleecker, 2001). These proteins share similar predicted extracellular domains, referred to as S domains, because they exhibit sequence similarity to the S locus glycoprotein (SLG), the first S locus–encoded gene isolated (Figure 2A) by Nasrallah et al. (1985). As expected for a receptor protein, SRK is an integral component of the plasma membrane (Stein et al., 1996; Dixit et al., 2000; Giranton et al., 2000), where it is displayed with its S domain on the outside of the cell and its kinase domain within the cytoplasm (Letham et al., 1999). At least one SRK allele (and possibly others) also produces soluble truncated forms of the SRK ectodomain, designated eSRKs (Giranton et al., 1995) (Figure 2A), apparently encoded by short transcripts that terminate within the first intron of the gene (Stein et al., 1991). The SRK protein is expressed specifically in the stigma epidermis, SRK transcripts accumulate concomitantly with the attainment of SI by mature stigmas (Stein et al., 1991, 1996), and SRK alleles can exhibit as much as 35% overall amino acid sequence divergence (Stein et al., 1991; Nishio and Kusaba, 2000; Kusaba et al., 2001a). Moreover, transformation with an SRK transgene resulted in the acquisition by transgenic stigmas of the corresponding SI specificity and the ability to reject pollen expressing the same S haplotype as that of the transgene (Takasaki et al., 2000). Significantly, the pollen of these transgenic plants did not acquire new SI specificity. This result confirmed previous data that suggested the existence of distinct S locus genes for pollen and stigma specificity. Self-compatible mutants of Brassica were known that exhibited defects in stigma SI function alone (Nasrallah, 1974; Hinata and Okazaki, 1986; Nasrallah et al., 1992, 1994) or in pollen SI function alone (Nasrallah et al., 2000). Moreover, both homology-dependent silencing of SRK (Conner et al., 1997) and expression of a dominant-negative form of SRK in transgenic plants (Stahl et al., 1998) had led to the stigma-specific breakdown of SI. The molecular cloning of SRK was facilitated by the previous isolation of SLG (Nasrallah et al., 1985), another highly polymorphic S locus gene that shares a high degree of sequence identity with the SRK ectodomain (Figure 2A) and is expressed at much higher The SLG glycoprotein is an component of the papillar cell wall et al., 1989), which does not specificity in the SI response to have an in SI. SLG the SI by the SRK transgene (Takasaki et al., 2000), and SLG was shown to the of SRK and its to in the stigma epidermis et al., 2000). SLG is not for a SI response. SLG did not the of the SI response in transgenic plants expressing the SRK transgene et al., 2001). at least two Brassica S et al., 2000) and the two S to et al., not an SLG gene. In these the SRK or by the corresponding eSRK molecules (Figure in recognition is the S locus Cys-rich protein SCR et al., and Nasrallah, 2000), also designated et al., et al., 2000; et al., 2001). The SCR gene is in genetic with SRK, as a result of the of S and a of at the S locus et al., 2000). The SCR gene exhibits S is expressed in and a of to amino The SCR gene is and for SI in pollen. SCR transcripts are in a of Brassica that exhibits a breakdown of SI et al., 1999). of Brassica plants for one S haplotype with an SCR allele derived from another haplotype in the acquisition by transgenic pollen of the SI specificity encoded by the transgene et al., et al., 2001). of stigma papillar cells with expressed SCR the of in et al., et al., 2001). The SCR protein been shown to to the pollen coat by et al., and by et al., 2001). a had been predicted based on the SCR expression et al., and Nasrallah, 2000; et al., 2000) and on a that the pollen SI to a component of the pollen coat (Stephenson et al., The site of SCR not been Pollen coat proteins in the or in Brassica SCR alleles to exhibit and as from the of SCR transcripts in the and in et al., and Nasrallah, 2000; et al., 2000; et al., 2001). In the SCR allele is expressed in and the SCR a allele is expressed only in the of et al., expression of SCR in the is for and expression of two SCR alleles in the is an for the of pollen SI specificity in The additional expression exhibited by another SCR and Brassica SCR alleles or to SCR in pollen SRK, SCR is a of a large gene that members in et al., 2001). A is the gene which genes pollen coat proteins of unknown function et al., exhibit not sequence to which are Cys-rich that are expressed in and plants et al., 2001). In they to have the same of as the et al., 2001). SCR alleles the Cys et al., 2000), and these form only function in although they also have As and the a first of to not interaction with specific by surface and form in SCR is a signaling with a different function and mode of it is to that a function directed at in was for recognition in the SI response. It that to the evolutionary have been in of different of 1999). It to the evolutionary of SCR because of the of the SCR gene. only Cys and one are conserved among the SCR sequences to in Brassica and and Nasrallah, 2000; et al., 2000; Kusaba et al., 2001a). In SCR sequences because of the of between the Cys The sequences and of SRK and SCR, as as the transgenic the that they act as a in the SI response. The model of SI is that SCR is a signal carried in the pollen coat that as a for the plasma the SCR protein to the stigmatic surface the by the pollen The papillar cell wall allows the of molecules of such as SLG et al., it is expected that the of SCR molecules this cell wall occurs within minutes of pollen–stigma contact. The interaction of SCR with the SRK ectodomain a signaling cascade that in the inhibition of self pollen tube the known of this signal transduction and mutations that the involvement of specific molecules in of this model are that SCR is the for SRK and that specificity in the SI response from specificity in or the activation of the S of SCR to the SRK ectodomain been demonstrated et al., 2001). this the ectodomain of was expressed as a in The and proteins were expressed in the as proteins that were in ectodomain had a high for it did not The in interaction was and did not additional molecules specific to the stigma or pollen It is that this in the absence of the S et al., and et al., 1991) two cell wall components of the stigma epidermis that exhibit sequence similarity to SLG and the SRK also did not the pollen coat protein which was shown to SLG in et al., and proteins also specifically to from pollen coat and to from respectively. as an the expected in pollen coat and in the that SCR its SRK as a in its and not from stigma also exhibited to soluble stigma proteins that likely represent also The of stigma SRK to its also was demonstrated in that used proteins encoded by the S 8 haplotype of Brassica et al., 2001). In this and demonstrated the of to stigma membrane The was to the protein and to a protein that to or possibly the of SLG shown to membrane associated et al., 2000). In to in the study by et al. the was in form and the did not to a form of the SRK S domain that was expressed in cells as a with the result by or modification of the protein in the expression studies are to the occurs in or dimeric form and which of these forms is in receptor It is that the two studies of interaction above both indicated an of SLG or eSRK with the receptor and The of this is not known. In the SLG those of SRK by of (Stein et al., and for SCR and this large of SLG SRK, these two proteins apparently in an at the papillar cell when in the of the cell wall and plasma membrane were (Stein et al., SLG and eSRK possibly by the interaction of SCR with SRK, as been shown for in models et al., The SRK protein is one of only plant single-pass receptor-like kinases have been The systems to the class of receptor-like These the protein and its et al., the protein, with its ligand, the et al., 2000), is for the of in et al., and the receptor which the and 2000). studies of these systems have been only and of plant receptor activation are understood. in receptor activation to the of and receptor In is known to the of resulting in of the kinase domains act as for specific different strategies to of the such as and are and one two receptor molecules and and 1999). such as et al., 1997) and et al., 1989), are and of their of receptor activation in plants are likely to as as those in between the and also as the and of SRK SLG, the of the receptor a receptor-like protein a extracellular domain and a transmembrane domain a kinase domain et al., 1999). both SCR and occur in higher in The forms a in et al., 1999). SCR was as an in pollen coat et al., although it is not known these represent the of SCR and this is for to An is that only the whereas SCR the extracellular domain of SRK a kinase domain et al., 2001). In this the interaction is similar to the of to its which does not a kinase domain et al., 2000), whereas both and et al., 2000; et al., 2001). SCR to the SRK ectodomain into of the and does this result in of the SRK The of a form of the to stigma membrane resulted in the of SRK et al., 2000). SRK was shown to within after et al., apparently by of the kinase (Giranton et al., 2000). the data are SRK is activated and it is in an in the absence of The activation of SRK been suggested to because SRK was in a and by to the of the SRK protein et al., 2001). It also been that SRK signaling by the of SCR to SRK and interaction with a because SRK were in stigmas in the absence of (Giranton et al., 2000). In one SRK was found to in (Giranton et al., 2000). This was inhibited by soluble proteins from stigma or by a protein that interacts with the SRK kinase domain et al., 1996; et al., and is known to the activity of kinases in systems et al., 2000). The inhibition of by was by the of pollen coat proteins from S pollen. These that the SRK kinase domain to the activation of the SI et al., to The of to SRK activation in of that did not involvement of et al., 2001). the study of SRK activation is in its and many from receptor studies that and receptor not result in receptor In only those forms of receptor that and and 1999). In the of molecules is for in the of the of molecules is for the of the receptor by and for receptor activation et al., that the of SRK is for is the of SCR to SRK to this and activation of the activation of SRK additional components from the pollen coat or papillar cell activation is by the of the and by the of to the activation is to cells within the domain of 2001). In the of SRK activation in the papillar cell is and likely to to a the of contact with a self pollen It been shown that the germination of a pollen is not by the of an pollen on the same papillar cell the pollen from SRK activation is to result not from of the surface of the stigma epidermal cell from to the site of contact with an pollen of SCR and of the SI Response. of isolated from a of expressing the S haplotype and from the and The was with SCR and with as a The the shows data from of S stigmas with pollen from S and expression of SCR a The absence of SCR transcripts in is with in pollen pollen tubes produced and a in SCR in in to pollen tubes produced One of these is that the of an barrier to self pollen the activation of SRK molecules and the of their at the site of pollen–stigma contact. The of the response on the of SCR molecules to this site by a pollen In the the number of SCR molecules from the into the and into the coat of pollen As a result, in those pollen that of SCR inhibited and those that or SCR protein the SI or by S associated with a expressed SCR An of SI in the Brassicaceae is that genetic interactions between S the expression of SI specificity in stigmas and pollen, a that for the mechanism of SI as as for the and of S in a interactions of or have been and these interactions can in stigma and pollen, with the activity of distinct stigma and pollen determinants of SI specificity. These interactions that SRK and SCR or not function of data on the molecular for S interactions were et al. that in the Brassica stigma are a of the SRK gene and that or was not with in SRK in a study of SI in the of S a activity in S a stigmas was not to in SRK expression et al., these studies did not the that is to in SRK protein it is possible that these genetic interactions between receptor or in the interaction or in the of of the SI response. been the interactions of S in pollen. In the S a haplotype is to the S haplotype in pollen, and pollen from S a plants exhibit S specificity et al., 2001a). SCR a which are expressed in the were by as much as in S a to S a et al., The mechanism of this is not understood. the interaction exhibited by the SCR a and SCR alleles in pollen is by expression of the SCR allele in S a resulting from of the SCR a allele in the and the of SCR a expression in The SCR a allele is the only allele to and it to this mechanism of to it is likely that the of expression of the SCR allele and expression of the SCR allele to many of S interactions in the pollen of and and SRK activation are transduced into the inhibition of self-related pollen is not understood. only the arm protein ARC1 et al., 1998) (Figure been conclusively as a component of the SRK signal transduction signaling the was by of its genetic to a of SI and by the that it was not expressed in plants for the et al., of two additional alleles by of plants and of that the gene was to represent the locus et al., 2001). ARC1 was in a as a protein that with the cytoplasmic domain of SRK et al., This which is by the arm repeats in the of ARC1, an SRK kinase domain and in the of ARC1 in et al., ARC1 transcripts are specifically in the a for ARC1 in Significantly, transgenic plants in which ARC1 transcripts were by the expression of an ARC1 transgene a breakdown of SI in the stigma and were not in pollen SI function et al., (Figure the breakdown of SI was only to ARC1 expression in transgenic stigmas or indicate that ARC1 is not the only for these a for ARC1 in SI. ARC1 is not understood. by the that ARC1 a U box et al., a in the et al., 1999). been shown to in the of signal transduction the of receptor signaling and receptor and the of a U box in ARC1 a for protein in SI. ARC1 is a of it is possible that ARC1 by activated SRK triggers its interaction with components of the and to the of an inhibitor of the SI response (Figure Other are because been shown to have to protein such as of proteins and their to molecular 1999). of mutants mutations in loci to the S locus and expressing ARC1 protein (Nasrallah et al., 2000) that as components are in the SI signal transduction The likely of this is by of the SI which that the of self pollen can occur at of pollen or pollen tube ingress into the papillar cell wall These that the signaling one molecular in the papillar cell and one the to the identity of signaling components activated by self-recognition and to the of pollen inhibition have been and cell studies of pollen tube in and are known to SI in high high and of the stigma with and of these the mechanism of pollen studies have on the of in SI. is known to a in pollen germination and pollen tube and et al., et al., which is by a in the papillar is by pollen 1993). It and by such as the protein that is expressed in the pistil and of Brassica and or the Brassica protein which is expressed specifically during pollen et al., 1999). is of because it is in the of mature pollen it into the pollen wall after pollen and it the surface of the pollen demonstrated that the pollen tube in a of from the and that this is germination and et al., et al., and of the pollen tube are to in this and it been suggested that an in in the pollen one of the by in the SI response of the the of pollen tube is associated with and the of a within the of the pollen tube et al., In Brassica a for in pollen was suggested by an study in which a in was in pollen during an et al., this result can using is not known. A for in the stigma SI response also been in the stigma the of at the site of pollen contact This is and is by the of pollen pollen coat and to the stigma et al., and 1999). of stigmas with an inhibitor of did not the ability of these stigmas to reject self pollen and In the of in the of transgenic Brassica expressing did not the SI response et al., it is that as a barrier to pollen tube Rather, it represent a of within the papillar In to for pollen et al., between and were in the of although the of was higher in papillar cells to pollen to those to pollen. In both and were at in membrane and membrane et al., is between different signaling and this likely signaling The inhibition of pollen tube in SI been with the inhibition of in et al., and 1999). is as for molecular between the signal and signaling in is for the of signaling with plant signaling the system in with proteins in a that its ligand, et al., 2000), protein and a protein that for signal transduction et al., 1999). is a of et al., et al., 1998) and et al., signal transduction and the protein is to function in the of of receptor SRK is not known to with a protein, at least one allele of SRK in et al., the of this not been The last have in our understanding of cell-to-cell in the SI response and of the specific interactions for the recognition of self pollen. The been for studies of pollen–stigma of the signaling system by studies of plant such as and is the evolutionary and to members of the large genes families that are to these and and and Bleecker, et al., 2001). the of this of genes a specific receptor with its this by a understanding of the polymorphic of genes the study of these systems of signal perception and response as as with signaling in and for the in in the is by the of the and the of
Source: The Plant Cell
DOI: 10.1105/tpc.010440
Institution: Cornell University
Language: English
Topic: Plant Reproductive Biology
Subfield: Molecular Biology
Domain: Life Sciences
Open Access status: bronze
OpenAlex ID: W2097452884