Molecular Plant Advance Access published online on May 16, 2008
Molecular Plant, doi:10.1093/mp/ssn023
A Dialogue between the Sirène Pathway in Synergids and the Fertilization Independent Seed Pathway in the Central Cell Controls Male Gamete Release during Double Fertilization in Arabidopsis
a Ecole normale supérieure de Lyon, Unité Mixte de Recherches 5667 Reproduction et développement des plantes, 46 allée d'Italie, 69007 Lyon cedex 07, France
b Centre for Integrative Genomics, University of Lausanne, Le Génopode, 1015 Lausanne, Switzerland
c Unite Mixte de Recherches IPMSV, CNRS/INRA/Unice, 400 route des chappes, Sophia Antipolis F-06903, France
d European Commission, Research Directorate General, Research Infrastructures (Unit B3), Office SDME 1/133, B-1049 Brussels, Belgium
e Temasek Life Sciences Laboratory, 1 Research link, National University of Singapore, Singapore 117604
1 To whom correspondence should be addressed. E-mail fred{at}tll.org.sg.
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Abstract |
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 TOP Abstract INTRODUCTIONRESULTSDISCUSSIONMETHODSFUNDING |
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Angiosperms sexual reproduction involves interactions between the two female gametes in the embryo sac and the two male gametes released by the pollen tube. The two synergids of the embryo sac express the FERONIA/SIRÈNE receptor-like kinase, which controls the discharge of the two sperm cells from the pollen tube. FER/SRN may respond to a ligand from the pollen tube. Alternatively, the interaction between FER/SRN and a ligand from the embryo sac may lead to a state of competence of the synergids allowing pollen tube discharge. Here, we report the new mutant scylla (syl) impaired in the control of pollen tube discharge. This mutant also produces autonomous endosperm development in absence of fertilization—a trait associated with the FERTILIZATION INDEPENDENT SEED (FIS) mutant class. This led us to identify autonomous endosperm in srn mutants and to demonstrate synergistic interactions between srn and the fis mutants. In addition, the fis mutants display defects in pollen tube discharge as in srn and syl mutants, confirming the interaction between the two pathways. Our findings suggest that pollen tube discharge is controlled by an interaction between the synergids expressing SRN/FER and the central cell expressing FIS genes.
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INTRODUCTION |
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TOPAbstractINTRODUCTIONRESULTSDISCUSSIONMETHODSFUNDING |
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Flowering plants have evolved a complex fertilization mechanism involving two sperm cells and two female gametes—the egg cell and the central cell (Berger, 2008). Two fertilizations take place in a coordinated manner and initiate seed development. The fertilized egg cell produces the embryo. The fertilized central cell develops as the endosperm, which nurtures embryo development. This peculiar mode of reproduction was termed ‘double fertilization’ and was first identified as a hallmark of Angiosperms biology at the end of the nineteenth century by L. Guignard (1899) and S. Nawaschin (1898). However, since its discovery, the cellular and molecular mechanisms involved in this unique reproductive process have remained rather enigmatic (Weterings and Russell, 2004). Recently, imaging the entire process of double-fertilization in vivo in Arabidopsis was achieved (Ingouff et al., 2007), and two major advances have been made in the past years: (1) the discovery of the FERTILIZATION INDEPENDENT SEED (FIS) pathway responsible for gamete cell cycle arrest (Berger et al., 2006), and (2) the identification of a potential signaling mechanism responsible for the male gamete release by the pollen tube (Punwani and Drews, 2008):
- (1) Cell cycle arrest in the Arabidopsis central cell is mediated by members of the conserved Polycomb-Group (PcG) complex FERTILIZATION INDEPENDENT SEED (FIS) (Berger et al., 2006). The Polycomb group complex FIS contains the SET domain protein MEDEA (MEA), the VEFS domains protein FERTILIZATION INDEPENDENT SEED 2 (FIS2), and the WD40 domain proteins FERTILIZATION INDEPENDENT ENDOSPERM (FIE) and MULTICOPY SUPPRESSOR OF IRA 1 (MSI1) (Guitton et al., 2004; Kohler et al., 2003). Loss-of-function mutations of FIS genes show autonomous onset of cell division in the central cell in the absence of fertilization (Chaudhury et al., 1997; Ohad et al., 1996). In addition, msi1 mutants show additional autonomous division in the egg cell, leading to a non-viable parthenogenetic embryo (Guitton and Berger, 2005). This suggests that distinct mechanisms control the arrest of the egg cell and of the central cell in the mature female gametophyte (Curtis and Grossniklaus, 2008).
- (2) Laser dissections of ovules from Torenia demonstrated the major role played by synergids in short-range attraction of the pollen tube (Higashiyama et al., 1998, 2001; Higashiyama, 2008). In Arabidopsis, the synergids also appear primarily responsible for the micropylar guidance from the entrance of the micropyle to the female gametophyte (Kasahara et al., 2005). After entering the embryo sac, the pollen tube stops its growth and discharges its contents, through interaction with the synergids. In-vivo observations suggested that the degeneration of one synergid is triggered only after pollen tube arrival (Rotman et al., 2003; Sandaklie-Nikolova et al., 2007) or pollen tube discharge (Higashiyama et al., 2000). Recently, molecular insights in this dialogue between the pollen tube and the female gametophyte have been obtained. Cessation of pollen tube growth in the female gametophyte requires the receptor-like serine/threonine kinase FERONIA, accumulated on the plasma membrane at the micropylar pole of synergids (Escobar-Restrepo et al., 2007). In absence of FERONIA in the synergids, the pollen tube grows and coils in the female gametophyte without releasing its content (Huck et al., 2003; Rotman et al., 2003). FERONIA sequence diverges quite markedly between species related to Arabidopsis (Escobar-Restrepo et al., 2007) and may provide an element of the interspecific reproductive barriers. The receptor-like kinase FERONIA may interact with a ligand provided by the pollen tube. Interestingly, peroxisomes in both male and female gametophytes also play a key role in pollen tube arrest, as suggested by the phenocopy of the sirène and feronia phenotypes observed in the mutant abstinence by mutual consent (amc), which is defective in a peroxin essential for protein import into peroxisomes (Boisson-Dernier et al., 2008). The calcium pump ACA9 on the plasma membrane of the pollen tube is also essential for pollen tube discharge, suggesting a contribution of calcium signaling to this process (Schiott et al., 2004). The pollen tube may provide signals to the synergids and respond to signals emanating from the female gametophyte, suggesting that additional male gametophytic mutants remain to be isolated to identify the ligand of the FERONIA receptor-like kinase. An alternative hypothesis is that the function of synergids is non-cell autonomous and requires a dialogue involving FERONIA with other cells of the gametophyte, leading to a degree of sexual maturity enabling the interaction with the pollen through a still unknown pathway. According to this hypothesis, the central cell or the egg cell may provide the FERONIA ligand.
- (2) Laser dissections of ovules from Torenia demonstrated the major role played by synergids in short-range attraction of the pollen tube (Higashiyama et al., 1998, 2001; Higashiyama, 2008). In Arabidopsis, the synergids also appear primarily responsible for the micropylar guidance from the entrance of the micropyle to the female gametophyte (Kasahara et al., 2005). After entering the embryo sac, the pollen tube stops its growth and discharges its contents, through interaction with the synergids. In-vivo observations suggested that the degeneration of one synergid is triggered only after pollen tube arrival (Rotman et al., 2003; Sandaklie-Nikolova et al., 2007) or pollen tube discharge (Higashiyama et al., 2000). Recently, molecular insights in this dialogue between the pollen tube and the female gametophyte have been obtained. Cessation of pollen tube growth in the female gametophyte requires the receptor-like serine/threonine kinase FERONIA, accumulated on the plasma membrane at the micropylar pole of synergids (Escobar-Restrepo et al., 2007). In absence of FERONIA in the synergids, the pollen tube grows and coils in the female gametophyte without releasing its content (Huck et al., 2003; Rotman et al., 2003). FERONIA sequence diverges quite markedly between species related to Arabidopsis (Escobar-Restrepo et al., 2007) and may provide an element of the interspecific reproductive barriers. The receptor-like kinase FERONIA may interact with a ligand provided by the pollen tube. Interestingly, peroxisomes in both male and female gametophytes also play a key role in pollen tube arrest, as suggested by the phenocopy of the sirène and feronia phenotypes observed in the mutant abstinence by mutual consent (amc), which is defective in a peroxin essential for protein import into peroxisomes (Boisson-Dernier et al., 2008). The calcium pump ACA9 on the plasma membrane of the pollen tube is also essential for pollen tube discharge, suggesting a contribution of calcium signaling to this process (Schiott et al., 2004). The pollen tube may provide signals to the synergids and respond to signals emanating from the female gametophyte, suggesting that additional male gametophytic mutants remain to be isolated to identify the ligand of the FERONIA receptor-like kinase. An alternative hypothesis is that the function of synergids is non-cell autonomous and requires a dialogue involving FERONIA with other cells of the gametophyte, leading to a degree of sexual maturity enabling the interaction with the pollen through a still unknown pathway. According to this hypothesis, the central cell or the egg cell may provide the FERONIA ligand.
We have identified the female gametophytic mutant scylla (syl), also deficient for pollen tube arrest and displaying a phenotype similar to that of srn mutant allele. However, syl and srn genetic locations are different and thus represent distinct mutations. We also observed autonomous endosperm development from syl ovules, suggesting a link between the fis pathway and the srn pathway, which we confirmed.
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RESULTS |
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Isolation of a New Mutant with Altered Pollen Tube Arrest
We performed a genetic screen in order to isolate mutants deficient in pollen tube reception and pollen tube arrest typical of the sirène class represented by the two alleles srn and fer. Plants from a population of Columbia (Col) wild-type seeds irradiated by gamma rays were used as pollen donors to fertilize wild-type ovules. We did not obtain male gametophytic mutants defective for fertilization amongst 2000 lines. However, we isolated mutant lines that showed more than 25% seeds arrested at early stages after self-fertilization. The line GM862 showed a phenotype similar to srn, fer, and amc. We tentatively named the mutation carried by GM862 scylla (syl).
Genetic Transmission of GM862
A M2 population from the self-fertilized syl M1 plant contained a proportion of 50% mutant plants producing 30–40% arrested seed and did not contain any plant-producing 60–80% arrested seeds, suggesting that the mutation could not be obtained as homozygous. After four backcrosses to wild-type plants, we estimated the genetic transmission of syl (Table 1). The syl mutation was fully transmitted by the pollen. In contrast, the transmission by the female gametes was strongly reduced (Table 1). We thus hypothesized that the line syl carried a single mutation causing female gametophytic defects. The transmission efficiency of syl from self-fertilized plants was even further reduced and the absence of homozygous syl plants suggested that the syl mutation may cause lethality in syl/syl embryos or seedlings. We constructed a mapping population from crosses between syl/+ (Columbia) with the wild-type accession Ler. Independent mapping (306 chromosomes) led to localize the mutation on chromosome 5 to an interval defined by the markers nga 225 and nga 249. This interval is distinct from the location of srn and fer and thus the line syl/+ likely carried a mutation distinct from previously identified mutation associated with a srn phenotype.
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Phenotypic Analysis
Ovules from syl/+ mutants did not show any obvious morphological defect but caused pollen tube arrest after various degrees of growth in the embryo sac micropyle (Figure 1A). All ovules from wild-type and from syl/+ plants expressed the genes FIS2 (Figure 1B; n = 234), a marker of differentiation of the central cell. We concluded that the mutation syl might not alter the development of the female gametophyte.
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Ovules from syl/+ plants pollinated with pollen expressing GUS under the LAT52 promoter either showed the release of GUS in the embryo sac, as in wild type (Figure 1C), or an arrested or coiled pollen tube (Figure 1D and 1E). The absence of pollen tube discharge in syl ovules was confirmed using aniline-blue staining of the pollen tube cell wall (Figure 1F and 1G). The proportion of ovules with a coiled pollen tube was 32% (n = 125). We concluded that the pollen tube discharge did not take place in syl ovules. When ovules from syl/+ plants were fertilized by wild-type pollen, a conspicuous coiling of the pollen tube was observed with DIC microscopy at the micropyle in 33% of ovules (Table 2). The percentage of ovules showing coiled pollen tubes did not increase in self-pollinated syl/+ plants and the phenotype was not observed in wild-type ovules pollinated using syl/+ plants. The observation of ovules with a coiled pollen tube only in crosses involving syl/+ plants as female confirmed that syl had an impact on female gametophyte development. The penetrance associated to this phenotype was of the same order as the TE of the syl mutation, indicating that the absence of discharge of the pollen tube caused by the syl mutation in ovule likely accounts for the lack of transmission of syl by the female gametophyte. The pollen coil was reminiscent of the phenotype caused by srn and fer mutations, although, in syl, the pollen tube could either stop at the micropyle (Figure 1A and 1G) or proliferate in an invasive manner in the embryo sac (Figure 1E and 1H) as in srn and fer. We also observed a high incidence of several pollen tube contacts per ovule (polysiphony) in self-fertilized syl/+ plants (Figure 1H; 5–15%, n > 300). Altogether, the lack of pollen discharge, followed by further pollen tube growth and polysiphony, indicate that the syl mutation belongs to the sirène (mermaid in French)-class mutation originally defined by the mutant sirène (Rotman et al., 2003) and its allele feronia (Huck et al., 2003). The name Scylla refers to a monstrous mermaid in Greek mythology, alluding to the fact that the female gametophyte lures the pollen tube.
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In seeds developing from syl/+ ovules fertilized by wild-type pollen, we also observed a low percentage of developing seeds with the pollen coil at the micropyle, containing developing endosperm with a few nuclei but no embryo (Figure 1I). This mode of development was reminiscent of autonomous endosperm development observed in fis-class mutants. To evaluate autonomous endosperm production in syl/+, we emasculated pistils and observed ovule development after emasculation in absence of fertilization. Wild-type fertilized seeds contain an embryo and an endosperm (Figure 2A) and wild-type emasculated ovules abort, still showing remnants of the nuclei of the central cell and the egg cell (Figure 2B). In unfertilized emasculated syl/+ flowers, we observed a proportion of 30% of enlarged ovules containing from two to 32 endosperm nuclei (Figure 2C and 2D; Table 3). We confirmed that proliferating tissue from the emasculated ovule has an endosperm identity, as it showed typical syncytial divisions and expressed the endosperm marker FIS2 (Figure 2E and 2F). Autonomous endosperm development has been observed in the fis-class mutants and was coupled with a maternal effect on endosperm development. In fertilized syl/+ siliques, we did not observe seeds carrying an embryo and endosperm showing a fis phenotype, suggesting that syl is not associated to a maternal effect. We concluded that the syl mutations causes a defect in embryo sac function leading to an absence of cell cycle arrest in the central cell and to an improper dialogue with the pollen tube, resulting in the sirène phenotype.
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Autonomous Development in srn Class Mutants
Observation of autonomous development in the syl mutant ovules led us to consider that autonomous endosperm development also takes place in the sirène mutant. We emasculated flowers from srn/+ and observed ovule development 3.5 days after emasculation (DAE). Although most ovules did not show any nucleus division in the central cell (Figure 3A), a fraction of srn ovules exhibited two to four nuclei in the central cells, indicative of autonomous endosperm development (Figure 3B and 3C). The very low penetrance associated with this trait (Table 3) explains why it was overlooked in previous studies (Huck et al., 2003; Rotman et al., 2003).
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To study whether the srn mutation is associated with the fis pathway, we studied the expression of the FIS genes MEA and FIS2 in srn/+ plants. All ovules from srn/+ plants homozygous for the transgene reporting MEA or FIS2 expression expressed MEA (Figure 3D) and FIS2 (Figure 3E), indicating that autonomous development in srn ovules was not caused by reduction of the expression of these genes. In addition, we observed expression of FIS2 in autonomous endosperm from srn ovules (Figure 3F). We constructed the double mutant srn/+;fis2/+ and compared the percentage of autonomous endosperm development with fis2/+ and srn/+ plants (Table 3). We observed a remarkable increase in the frequency of enlarged ovules, with autonomous endosperm reaching 43.4% in the double mutant plants grown in parallel with the fis2/+ (34.4%) and the srn/+ plants (2.6%). This percentage indicates a synergy between the fis2 and the srn mutations (chi-squared test, P > 0.95).
The FIS Class Mutant msi1 Shows a srn Phenotype
The synergy between the fis and the srn pathway suggested that fis mutants could also exhibit the srn phenotype. We choose to investigate this possibility using the mutant msi1, which produces autonomous endosperm with high penetrance. In contrast to the arrested development in wild-type emasculated ovules (Figure 3A), msi1-emasculated ovules enlarge with autonomous development of the endosperm within 1.5–4 DAE (Figure 4B). The autonomous embryo development is visible only after 4 DAE (Guitton and Berger, 2005). We observed srn phenotype at a low frequency in self-fertilized msi1/+ plants (1.4%, n = 379) (Figure 4C).
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We reasoned that the srn phenotype might be caused by the onset of autonomous development of the central cell. We emasculated msi1/+ plants and pollinated msi1/+ plants at 1.5 and 3.5 DAE. Delayed pollination for 1.5 DAE caused a marked increase in the srn phenotype coupled with autonomous development (Table 2). The percentage diminished when pollination was performed at 3.5 DAE, which may result from the decreased attraction of pollen tubes by 3.5-DAE-old ovules (Table 2). At 3.5 DAE, we could observe autonomous endosperm development and the autonomous elongation of the zygote (Figure 4D). Interestingly, the srn phenotype was also observed with increased frequency with the delayed fertilization of emasculated wild-type ovules (Table 2). We concluded that there is a clear link between the srn phenotype and the autonomous endosperm development in msi1 mutants.
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DISCUSSION |
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We show that the fis mutant msi1 exhibits a phenotype similar to that described in the mutants srn and fer with a prevention of pollen tube arrest leading to uncontrolled pollen tube growth in the micropyle with potential invasion of the embryo sac and polysiphony (Huck et al., 2003; Rotman et al., 2003). Reciprocally, we observe that the srn mutant exhibits autonomous endosperm development in synergy with the fis pathway. In addition, we identify the mutant syl, which exhibits the srn phenotype and also produces autonomous endosperm. The syl mutant thus combines phenotypic traits typical of the fis and the srn mutant classes. We thus conclude that the pathway linked to autonomous endosperm development triggered by the fis mutations is associated with the pollen tube arrest caused by the sirène mutations.
What is the origin of autonomous endosperm development in srn and syl mutants? Autonomous development in fis mutants is caused by the loss of function of FIS genes in the central cell. The expression of FIS genes in srn and syl does not favor the hypothesis of a down-regulation of the FIS gene expression in the central cell. However, we do not know how the expression of FIE and MSI1 are affected in syl and srn mutants. An alternative hypothesis involves a non-cell autonomous mechanisms. SRN/FER encodes a receptor-like kinase expressed specifically in the synergids (Escobar-Restrepo et al., 2007). It is thus possible that FERONIA is involved in signaling inside the female gametophyte, leading to a proper maturation of the central cell and preventing unwanted premature division. The absence of the srn-dependent signaling would thus cause initiation of central cell development and improper arrest of the pollen tube. A similar interaction between the central cell and the synergids may be involved in pollen tube guidance. Although the synergids have been clearly shown to be the major player in the pollen tube guidance (Dresselhaus, 2006; Higashiyama, 2008), the gene CENTRAL CELL GUIDANCE (CCG) expressed specifically in the central cell has been isolated for its role in pollen tube guidance (Chen et al., 2007). This gene encodes a general transcription factor and may affect the production of an attractant further processed by the synergids. Alternatively, CCG may be essential for interactions between the central cell and the synergids, allowing differentiation of the synergids and the production of the pollen tube attractant. It is thus likely that communication between the central cell and the synergids is essential for proper gametophyte function in pollen tube attraction. Likewise, our data suggest that communication between the central cell and the synergids may be essential for proper arrest of the pollen tube by the female gametophyte.
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METHODS |
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Plant Material and Growth Conditions
Seeds of all wild-type ecotypes Col-0, Ler, and C24 were obtained from the Arabidopsis Biological Resource Center (www.Arabidopsis.org). The marker lines carrying the MEA–GUS and the FIS2–GUS reporters (Luo et al., 2000) and LAT52–GUS (Twell et al., 1991) were a kind gift from Abed Chaudhury and Sheila McCormick, respectively. The lines msi1-2, fis2-6 (Guitton et al., 2004) and srn (Rotman et al., 2003) were previously described from our laboratory.
After 3 d at 4°C in the dark, seeds were germinated and grown on soil. Plants were cultured in a growth chamber under short days (8 h of light at 20°C/16 h of dark at 16°C; 60–70% hygrometry) until rosettes were formed. Plants were transferred to long days at 20°C (14 h of light/10 h of dark) to induce flowering.
For crosses and autonomous seed development, anthers were removed 1–1.5 d before anthesis under greenhouse conditions. Anthesis corresponds to the time when flowers open and self-pollination occurs in Arabidopsis. Pollination of emasculated pistils was done at the forecasted day of anthesis or at several days after emasculation (DAE). In order to favour autonomous endosperm development, plants were grown under continuous light at 22°C.
Microscopy and Image Processing
Ovules and developing seeds were isolated from individual siliques at different stages of development. Seeds were mounted in Hoyer's medium and observed microscopically using differential interference contrast (DIC) optics (Boisnard-Lorig et al., 2001). GUS staining was previously described (Ingouff et al., 2005). Aniline-blue staining was performed as described previously (Rotman et al., 2003). Images were acquired with a DXM1200F digital camera (Nikon, Tokyo, Japan) and processed using Metamorph (version 6.2; Universal Imaging, CA, USA).
Genetic Mapping
The line GM 862 (Col-0 accession background) was obtained from the genetic screen of a 
-ray mutagenized Arabidopsis seeds, as previously described (Guitton et al., 2004), and were crossed with wild-type Landsberg erecta (Ler) to generate F1 plants heterozygous for polymorphic markers between Col and Ler. The F1 mutant plants were allowed to self-generate F2 mapping populations. A small mapping population of 153 F2 plants from the GM862 line was analyzed. Markers for mapping were designed using the polymorphisms of the Cereon (www.Arabidopsis.org/Cereon/index/html) online database.
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AEG and NR were supported by a Ph.D. grant from the Ministry of Research. MG was supported by a post-doctoral grant supported by the Action Concertée Incitative.
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Acknowledgements |
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Most of the work was produced at the Unité Mixte de Recherches Reproduction et Développement des Plantes and was supported by the INRA (FB) and CNRS (JEF).
No conflict of interest declared.
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Notes |
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2 These authors contributed equally to this manuscript.
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