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(American Journal of Botany. 2008;95:1426-1436.) doi: 10.3732/ajb.0800110 © 2008 Botanical Society of America, Inc. |
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Evolution and Phylogeny |
2 Université Paris-Sud, Laboratoire Ecologie Systématique et Evolution, UMR8079 CNRS, AgroParisTech, 91405 Orsay cedex, France 3 Jodrell Laboratory, Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3DS, UK 4 UMR Génétique Végétale, INRA, AgroParisTech, CNRS, Gif-sur-Yvette, 91190, France
Received for publication 25 March 2008. Accepted for publication 10 August 2008.
ABSTRACT
This paper presents the first broad overview of three main features of microsporogenesis (male meiosis) in angiosperms: cytokinesis (cell division), intersporal wall formation, and tetrad form. A phylogenetic comparative approach was used to test for correlated evolution among these characters and to make hypotheses about evolutionary trends in microsporogenesis. The link between features of microsporogenesis and pollen aperture type was examined. We show that the pathway associated with successive cytokinesis (cytoplasm is partitioned after each meiotic division) is restricted to wall formation mediated by centrifugally developing cell plates, and tetragonal (or decussate, T-shaped, linear) tetrads. Conversely, much more flexibility is observed when cytokinesis is simultaneous (two meiotic divisions completed before cytoplasmic partitioning). We suggest that the ancestral type of microsporogenesis for angiosperms, and perhaps for all seed plants, associated simultaneous cytokinesis with centripetal wall formation, resulting in a large diversity in tetrad forms, ranging from regular tetrahedral to tetragonal tetrads, including rhomboidal tetrads. From this ancestral pathway, switches toward successive cytokinesis occurred among basal angiosperms and monocots, generally associated with a switch toward centrifugal intersporal wall formation, whereas eudicots evolved toward an almost exclusive production of regular tetrahedral tetrads. No straightforward link is found between the type of microsporogenesis and pollen aperture type.
Key Words: comparative analysis • correlated evolution • cytokinesis • intersporal wall formation • microsporogenesis • pollen aperture type • tetrad form
Microsporogenesis, or male meiosis, is a key step of the life cycle in plants because this process leads to the formation of haploid microspores that will ultimately give rise to the male gametophyte. In seed plants, the male gametophyte is the pollen grain, a highly reduced organism that is surrounded by an extraordinarily resistant wall made of sporopollenin. The pollen wall of flowering plants presents sculpturing patterns that vary among taxa, and it is interrupted in places by areas called apertures, which may differ in shape, number, and distribution on the pollen grain surface (aperture pattern). The apertures are the first morphological feature of the pollen grain appearing during pollen ontogeny (Blackmore and Barnes, 1990
). They are often visible in the late tetrad stage, which allows observation of the position of the apertures relative to the center of the tetrad, even when the mature pollen is shed in monads. The systematic value of pollen morphology is widely recognized and has been so for decades (see, for example, Erdtmann, 1952), and it is interesting to note that the first steps of pollen ontogeny, i.e., microsporogenesis, also present features that are of systematic significance. The characteristic of microsporogenesis most described is the type of cytokinesis or cell division, and publications mentioning this trait date back to the 19th century (for example, Guignard, 1897). During microsporogenesis, cell division can be either simultaneous, whereby the two meiotic divisions are completed before cytoplasmic partitioning, or successive, where the cytoplasm is partitioned after each meiotic division.
So far, cytokinesis is the only trait of microsporogenesis for which variation has been studied at a broad taxonomic scale, using a phylogenetic approach (Rudall et al., 1997; Furness and Rudall, 1999, 2000; Furness et al., 2002). Figure 1 shows the distribution of cytokinesis on the latest version of the monocot ordinal phylogeny, stressing the variation observed among and within orders. However, cell division is not the only feature of microsporogenesis that varies across angiosperms. Other features include the way intersporal walls are formed and the shape of resulting tetrads. Until recently, descriptions of intersporal wall formation were available for a limited number of species only, belonging to the monocots (Waterkeyn, 1962; Chikkannaiah, 1963; Longly and Waterkeyn, 1979; Periasamy and Amalathas, 1991), to basal angiosperms (Farr, 1918; Sastri, 1957, 1962; Hotchkiss, 1958; Hayashi, 1960; Sampson, 1963; Bhandari and Venkataraman, 1968; Sampson, 1969; Dinis and Mesquita, 1993; González et al., 2001; Tsou and Fu, 2002) and to the eudicots (see, for example, Bolenbaugh, 1928; Horner and Lersten, 1971; Albertsen and Palmer, 1979; Blackmore and Barnes, 1988, 1995), bearing in mind that basal angiosperms and eudicots were formerly classified in the dicots. The common view presented in papers or books on embryology was that wall formation occurred via centrifugal cell plates in the case of successive cytokinesis, whereas it occurred by centripetally growing furrows, meeting in the center of the microsporocyte, in the simultaneous situation (Bhojwani and Bhatnagar, 1974; Rangaswamy et al., 2001). However, evidence from studies conducted in basal angiosperms (for example, in Annona: Sastri, 1957; Magnolia: Hayashi, 1960; Laurelia: Sampson, 1969), and more recently in several families of monocots (Penet et al., 2005; Nadot et al., 2006a; Sannier et al., 2006), has demonstrated that other combinations exist. These studies indicate that variation in microsporogenesis does not necessarily have an influence on the aperture type of the resulting pollen grains.
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Using a data set combining previously published descriptions of microsporogenesis obtained in our laboratory (Ressayre, 2001; Ressayre et al., 2003, 2005; Penet et al., 2005; Nadot et al., 2006a, b; Sannier et al., 2006, 2007) and new unpublished data, we analyze in this paper the variation in microsporogenesis across a range of angiosperm species, to address the following questions: to what extent does the inference "tetragonal/decussate tetrad form = successive cytokinesis + centrifugal wall formation; and tetrahedral tetrad form = simultaneous cytokinesis + centripetal wall formation" hold? Is there a straightforward relationship between the type of microsporogenesis and the apertural type?
The analysis was conducted using the comparative method. Phylogenetic comparative methods (PCMs) are statistical tools that were originally developed by evolutionary ecologists to test hypotheses of adaptation. Correlated evolution between a morphological and an ecological character in a set of species is examined, taking into account the phylogenetic background of these species (Harvey and Pagel, 1991; Cézilly et al., 2000; Chapman et al., 2006; Summers et al., 2007). By this means, we can distinguish correlates due to adaptation from historical correlates. PCMs are also relevant in looking at correlations between morphological characters (Cubo and Arthur, 2000) as a way to detect developmental constraints, i.e., factors limiting the potential range of forms into which an organism can grow (Rudall and Bateman, 2003; Penet et al., 2007), which is our purpose here.
MATERIALS AND METHODS
Observations on microsporogenesis
Four features of microsporogenesis were recorded for 65 species: cytokinesis, intersporal wall formation, tetrad form, and callose ring. In addition, pollen aperture type was recorded for all species examined. Table 1 lists the characters states that we defined for each character except for the aperture type. When more than two states were defined for a character, a binary coding was additionally proposed, for the purpose of comparative analysis (described later). For the character tetrad form, two alternative binary codings were used, named tetrad form 1 and tetrad form 2. A third coding, rhomboidal, was additionally defined to account for the absence/presence of rhomboidal tetrads, a form in which all microspores are in the same plane and are separated by five division planes. Character states are illustrated in Fig. 2. The list of species, their taxonomic position, and the character states for microsporogenesis plus pollen aperture type are given in Appendix S1 (see Supplemental Data with online version of this article). We decided to include in this data set only information obtained in our laboratory to have homogeneous data, all observations were of tissue stained in the same manner (Ressayre, 2001). Also, descriptions of the type of cytokinesis that we found in the literature were not always accompanied by illustrations, and although we trust the various works published on microsporogenesis, we preferred to base this study only on information for which we could produce visual evidence.
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), following the topology of published phylogenies. Most phylogenetic information was obtained from the Angiosperm Phylogeny Website (Stevens, 2008). Additional resolution was necessary for Xanthorrhoeaceae s.l. (Devey et al., 2006), Iridaceae (Reeves et al., 2001; Goldblatt et al., 2006), Bromeliaceae (Crayn et al., 2004), and for palms (Asmussen et al., 2006). Branch lengths could not be taken into account since the tree was based on topologies obtained from heterogeneous data sets. They were attributed a default value of one. Characters were optimized on the tree using maximum parsimony or reconstructed using maximum likelihood, as implemented in Mesquite.
Tests of correlated evolution
The comparative analyses were carried out using the maximum likelihood (ML) and the Markov chain Monte Carlo (MCMC) methods implemented in the Discrete option of BayesTraits (available from http://www.evolution.rdg.ac.uk), both based on a continuous-time Markov model. The ML approach uses a likelihood ratio test (LTR) to examine correlated evolution between pairs of binary traits on a phylogeny, by calculating the likelihood of two models applied to the data (Pagel, 1994, 1999). One model allows traits to evolve independently (H0), whereas the other one (H1) assumes correlated evolution between traits (Fig. 3). If the latter model fits the data better than the first, which is evaluated by the likelihood ratio statistic LR = –2loge[L(H0)/L(H1)], the characters are considered to be correlated. The LR is asymptotically distributed as a 
2 variable with df = 4 (this corresponds to the difference in the number of parameters between the dependent and independent models). The LRT (I|D) was performed for nine combinations of binary characters, as listed in Table 2. The MCMC approach is a Bayesian method that can be used for investigating correlated evolution between two traits, by seeking the best fitting models that describe their joint evolution on a phylogeny (Pagel and Meade, 2006). We used the Reversible-Jump MCMC option to select the best fitting models of trait evolution for the same nine combinations of binary characters. Analyses were based on 20 200 000 iterations, with a ratedev of 10 (dependent model) or 8 (independent model), and an exponentially distributed hyper prior (seeded from a uniform 0–30 distribution) to allow for variation in rate coefficients among iterations. The first 200 000 iterations were discarded (burn-in), and the remaining 20 000 000 were sampled every hundredth iteration, resulting in 200 000 sample points. The log-harmonic mean of the likelihoods of the models explored was compared between two runs: one allowing for correlated evolution ("dependent" option) and the other with a constrained model of evolution ("independent" option). The test statistic that evaluates the relative fit of the two models is the Bayes Factor, 2(log[harmonic mean(better model)] – log[harmonic mean(worse model)]).
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Character optimization
Characters were optimized on a composite tree obtained from various published phylogenies and including only the species examined in this study. Figure 4 shows the composite tree on which the evolution of pollen aperture type was optimized using the MP method. Due to the presence of polymorphism in some taxa, the ML method could not be used. The ancestral state inferred for the angiosperms was the monosulcate type, corroborating the general view in palynology (based on the fossil record [Doyle, 2005]) according to which the aperture evolved from an ancestral single sulcus toward several furrows or pores in the eudicots (also named tricolpates, in reference to the main synapormorphy of this clade). Multiple apertures also evolved in the monocots, but the feature was derived and homoplastic within the clade, having evolved independently in unrelated families, for example, Bromeliaceae or Araceae, in which it should be noted that the dominant morph type has a single aperture (PalDat website pages, respectively, http://paldat.botanik.univie.ac.at/index.php?page=search&mode=tab_r&offset=0; http://paldat.botanik.univie.ac.at/index.php?page=search&mode=tab_r). Trichotomosulcate pollen, i.e., pollen with a single aperture in the shape of a three-branched furrow, was found only in the monocots, generally in association with monosulcate pollen: such a situation was found in three unrelated taxa in our sample, namely, the Iridaceae (Sisyrinchium), Hemerocallidaceae (Dianella), and Arecaceae (Gaussia). However, this is an artifact of our sampling because trichotomosulcate pollen also occurs as a small percentage with monosulcate pollen in some basal angiosperms, especially Canellaceae (Sampson, 2000). Only one taxon in our sample (Phormium, Hemerocallidaceae) exclusively produced pollen grains of the trichotomosulcate type, which reflects the fact that the production of trichomosulcate pollen without monosulcate pollen associated is quite rare—except in palms (Harley and Baker, 2001).
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Tests of correlated evolution
Simple 2 tests of correlations between pairs of binary characters performed on contingency tables (number of each type of combination of character states, i.e., 00, 01, 10 11) (Appendix S2, see Supplemental Data with online version of this article) showed that cytokinesis was highly correlated with all other characters: intersporal wall formation, presence/absence of a callose ring, and tetrad form (whatever coding was used). To test whether the associations between characters (for example, type of cytokinesis and type of wall formation) that were observed by visually comparing the trees were statistically significant and not due only to common ancestry, comparative analyses between pairs of binary characters were performed using the LRT and the MCMC method (Table 2). Among the 11 combinations of characters examined (the combination "cytokinesis/rhomboidal" was not examined), six pairs were found to be significantly correlated: the evolution of cytokinesis was correlated with the evolution of intersporal wall formation and tetrad form 1 and 2; intersporal wall formation was correlated with tetrad form 1 and rhomboidal; and callose ring was correlated only with rhomboidal tetrads. No temporal order or contingency (tested by constraining some of the parameters in the dependent model) could be detected among the transitions. Table 2 also gives the most probable ancestral combinations of character states as given by the ML and the MCMC methods. According to these probabilities, the ancestral microsporogenesis (for angiosperms and Ginkgo) had simultaneous cytokinesis occurring through centripetal wall formation, resulting in a mixture of various tetrad forms (including rhomboidal tetrads), and a callose ring was present.
DISCUSSION
Variation in microsporogenesis
This study, based on a large sample of species representing some of the main clades recognized in the monocots (with outgroups taken from basal angiosperms and eudicots), is the first broad-scale examination of the main features of microsporogenesis, and not only of the type of cell division (cytokinesis). It emphasizes previously published results focused on the Asparagales and the palm family (Penet et al., 2005; Sannier et al., 2006) that outlined the unexpected diversity that could be observed in these groups. Figure 6 summarizes the various associations that were observed among the main characters studied, i.e., type of cytokinesis, type of intersporal wall formation, and tetrad form. Contrary to simultaneous cytokinesis, which can be associated with any type of wall formation and tetrad form, successive cytokinesis is associated only with tetragonal (and related) tetrads and is usually associated with centrifugal wall formation. There is only one exception in Magnolia, where it is associated with centripetal wall formation.
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; Farr, 1918; Hayashi, 1960), who interpreted the type of cytokinesis as a special case of simultaneous cell division. In the species of Magnolia studied (M. tripetala L., Farr, 1918; M. liliflora Desr., Hayashi, 1960; M. soulangeana Soul.-Bod., this study; and M. stellata [Siebold & Zucc.] Maxim. [S. Nadot, unpublished data]), the cytoplasm is partially separated after the first nuclear division by a furrow of callose growing centripetally and orthogonally to the meiotic spindle. This furrow is arrested and completed only after the second nuclear division has taken place. No ephemeral cell plate is formed contrary to previous reports (Guignard, 1897). The centripetally growing furrows that divide the nuclei resulting from second meiotic division are completed after the completion of the first furrow. Cytokinesis is therefore intermediate between simultaneous and successive and was coded as such in this paper (Appendix S1 in online Supplemental Data; Fig. 5A). A similar situation was observed in Liriodendron tulipifera (Guzzo et al., 1994) suggesting that this type of microsporogenesis evolved in the common ancestor of all Magnoliaceae. It was also recorded for at least two species of Annonaceae (Sastri, 1957). In Laurelia novae-zelandiae (Monimiaceae), a furrow is formed at the end of meiosis I, and the cytoplasm is completely partitioned at the end of meiosis II like in Magnolia, but in this case by centrifugally growing cell plates (Sampson, 1969). For the binary coding, we chose to interpret this type of cell division as a special type of successive, rather than simultaneous cytokinesis, considering that the nuclei resulting from the first meiotic division are effectively separated as in the true successive type.
Simultaneous cytokinesis
Contrary to successive cytokinesis, the simultaneous type of cell division was found to occur through either centripetal or centrifugal wall formation. Variation in the latter character can occur at the intrafamilial level because both types of wall formation associated with simultaneous cytokinesis occur in the Arecaceae. In the species examined, simultaneous cytokinesis could result in a wide variety of tetrad forms, often produced within the same individual. This characteristic has already been noted for the Piperales (González et al., 2001), which belong to the magnoliids. When correlation tests were performed among the binary characters without phylogenetic correction, most characters were found to be associated, except for wall formation and tetrad form 2, suggesting no link between the type of intersporal wall formation and the exclusive production of tetrahedral tetrads.
Multistate vs. binary coding
It should be noted that coding a multistate character as binary necessarily implied a certain loss of information. Concerning tetrad form, this loss was partly made up by the use of two different codings, one accounting for the exclusive production of tetrads with three division planes (the so-called tetragonal state in the binary coding tetrad form 1) and the other accounting for the exclusive production of tetrads with six division planes (called tetrahedral in the character tetrad form 2).
Overall, the correlation tests suggest that constraints may exist in the developmental pathway. However, one can argue that testing correlations among related species without taking into account their phylogenetic background introduces bias in the result. The correlated traits may have each evolved independently in the common ancestor of all species, which then share these traits because of common ancestry and not because of a link between the traits (adaptation or developmental constraints, for example).
Correlated traits in microsporogenesis
To distinguish historical correlates from correlates due to developmental constraints among the traits of microsporogenesis, correlation tests were performed between the same pairs of traits of microsporogenesis, this time taking into account the phylogenetic background of the species examined. A difference was found concerning the character callose ring; it was correlated with all other characters without considering the phylogeny, but these correlations were somewhat lost in the phylogenetic comparative analyses except for the association with rhomboidal tetrads, which remained significant. This stresses the advantage of using such an approach for testing correlations. In the present situation, the loss of correlations corresponds probably to the fact that at least for one of the characters, taxa presenting the same character state are not independent (i.e., are phylogenetically related).
The results were slightly different between the likelihood ratio test and the MCMC method concerning two of the associations. The correlation between wall formation and tetrad form 2 on the one hand, and tetrad 1 and callose ring on the other hand, were not supported by the LR test although positive evidence for the correlated model was found with the MCMC method. However, the values of the log-Bayes factor for both situations are close to two (lowest value for interpreting the result as positive evidence for the dependent model), which corresponds to fairly weak support for the correlation. This weak support suggests that the exclusive production of tetrahedral tetrads can take place in the context of any type of wall formation (whereas tetragonal and related tetrads are mostly associated with centrifugal wall formation) and that the presence of a callose ring is not particularly associated with tetragonal or tetrahedral tetrads. However, a significant correlation between rhomboidal tetrads and a callose ring was found. Concerning the callose ring, few data are available from the literature because this feature had never been examined for a sizeable number of species. It has been suggested that in Iris and Tritonia (Iridaceae) the callose ring may constrain the tetrad form to tetragonal (Penet et al., 2005). The results obtained here do not allow generalization of this hypothesis to all species possessing a callose ring in the early stages of microsporogenesis. Interestingly, a well-supported correlation was found between the presence of rhomboidal tetrads and centripetal wall formation, suggesting perhaps the existence of a constraint preventing the formation of five division planes among nuclei when wall formation takes place centrifugally. There is one exception in our sampling (and to our knowledge), the palm family, the only taxon in which centrifugal wall formation can lead to rhomboidal tetrads.
Although some of the correlations between characters were strongly supported (for example, cytokinesis and wall formation, cytokinesis and tetrad form 1, wall formation and tetrad form 1, and wall formation and rhomboidal tetrads), both methods failed to detect clearly contingency or temporality in the evolution of one character vs. the other. Contradictory results were obtained not only for the transition parameters with the LR test (when the constrained dependent model was compared to the unconstrained model), but also with the MCMC method between runs and between iterations within the same run. This contradiction can be interpreted in two different ways. One possibility is that the two characters tested always change states simultaneously, for example from (0,0) to (1,1), and there is no intermediate state (0,1) or (1,0) (see Fig. 3). The other hypothesis may be that transitions from the initial state toward the final state occur through (0,1) or (1,0), but the number of transitions in each case is not sufficient to be statistically significant, although globally a correlation exists between the two characters. The two hypotheses may not necessarily be exclusive. Looking at the mirror trees corresponding to the pairs of characters that are significantly correlated (Appendix S3, see online Supplemental Data), assuming that the ancestral states inferred for the characters are more or less reliable (discussed in the next paragraph), supports these explanations. If we take for instance the pair cytokinesis and tetrad form 1, we can see that most transitions from simultaneous to successive cytokinesis and from mixed tetrad forms toward tetragonal tetrads [i.e., from (1,1) toward (0,0)] occur simultaneously, with at least two cases where a transition in tetrad form 1 is not associated with a transition in cytokinesis. If we consider now the pair wall formation and tetrad form 1, it appears that several types of transitions can be found, either directly from (1,1) to (0,0), or from (0,1) to (0,0) or from (1,0) to (1,1), showing lability in the two characters.
Ancestral states
The phylogenetic comparative methods that were used in this paper (ML and MCMC approaches) have the advantage of making it possible to test hypotheses about trait evolution without reconstructing ancestral states. Indeed, parameters of trait evolution are estimated by summing the likelihood over all possible states at each node of the tree (Pagel, 1994), consequently taking into account uncertainty in ancestral state reconstructions. This method for estimating parameters of trait evolution is particularly valuable in our case because bias in our taxonomic sampling (in monocots, Arecales, and Asparagales are better represented than other orders) in turn can potentially introduce bias in the inference of ancestral states, which is very probably the case for the type of cytokinesis. The ancestral state reconstructed for monocots using maximum parsimony (or ML) is simultaneous cytokinesis, which contradicts a previous study that proposed the successive type as ancestral for monocots (Furness and Rudall, 1999), based on much wider taxonomic sampling. Such bias is consequently likely to exist for the binary character tetrad form 1, which would be expected to have the state tetragonal as a consequence of successive cytokinesis, whereas it has the state tetrahedral and mixed for the ancestor of the monocots in the current study. The ancestral state inferred for the corresponding multistate character with ML is, however, predominantly tetragonal. Also, wall formation should be ancestrally centrifugal, which is the state expected with successive cytokinesis. However, in spite of these biases in ancestral state reconstruction for the monocots, we ascertained that this had no impact on the resulting correlations among characters by forcing the deepest nodes of the monocot tree to adopt the state 0 for all characters. We can therefore conclude that correlations found among characters reflect actual trends in the traits of microsporogenesis studied. We also think that the ancestral states for the deepest nodes of the tree are less biased and may well reflect the actual ancestral states for eudicots, angiosperms, and for seed plants, at least for the type of cytokinesis and the tetrad form, as indicated by previous studies (Huynh, 1974; Furness et al., 2002; Furness and Rudall, 2004). The successive cytokinesis found in Amborella (Tobe et al., 2000), identified as the first branching angiosperm, would then be derived. The simultaneous type of cytokinesis may even be ancestral at the level of embryophytes, since it was observed in bryophytes (Brown and Lemmon, 1988, 1991; Shimamura et al., 1998) although mediated by a centrifugally developing phragmoplast. The records of intersporal wall formation available from the literature seem to indicate a certain lability of this feature in basal angiosperms. In Laurales, successive cytokinesis mediated by centrifugal cell plates was noted in Cassytha from the Lauraceae (Sastri, 1962), although with no illustration of the developing walls. In addition, the record of tetrahedral tetrads in C. pubescens suggests that simultaneous cytokinesis probably occurs in this species, perhaps in combination with the successive type. Intersporal wall formation mediated by centrifugal cell plates, and simultaneous cytokinesis was noted in species from Austrobaileyales, namely, Illicium religiosum, Kadsura japonica, and Schisandra nigra (Hayashi, 1960). A detailed study of intersporal wall formation in basal angiosperms will be necessary to identify more precisely the state that was present in the ancestor of angiosperms.
Aperture type and microsporogenesis
Apertures are the first elements of pollen ornamentation to be established and are often visible in the late tetrad stage (Blackmore and Barnes, 1990), suggesting that the initiation of aperture formation should take place during microsporogenesis. It has been shown in Lilium and tobacco that the position of the apertures is linked with the orientation of the meiotic spindle (Heslop-Harrison, 1971; Sheldon and Dickinson, 1983, 1986; Ressayre et al., 2002). No direct correlation was found between pollen aperture type and cytokinesis type (successive or simultaneous) in a survey of monocots by Furness and Rudall (1999). No direct link between aperture type and cytokinesis or intersporal wall formation emerges from the present work because monosulcate pollen can be obtained with almost any combinations of these two characters, as had already been shown in the Asparagales (Penet et al., 2005). For example, monosulcate pollen results from successive cytokinesis and centripetal wall formation in Magnolia, simultaneous cytokinesis and centripetal wall formation in Nuphar, simultaneous cytokinesis and centrifugal wall formation in Veitchia, and from successive cytokinesis and centrifugal wall formation in Fosterella. Conversely, these combinations can result in other aperture types. On the other hand, tetrad form probably plays a role in aperture pattern determination, as suggested by the observation that tricolpate pollen grains in eudicots are always associated with regular tetrahedral tetrads, like the trichotomosulcate pollen of Phormium and Dianella in the monocots (Rudall et al., 1997). There is also evidence that callose deposition on intersporal walls after the second meiotic division (not recorded in the present paper) has an influence on aperture orientation (Ressayre, 2001; Ressayre et al., 2005), which is determined by the last points of contact among the microspores (Wodehouse, 1935; Blackmore and Crane, 1998). Interestingly, monoaperturate pollen can also be obtained in the absence of a tetrad stage (Periasamy and Amalathas, 1991). It appears then that the tight link between aperture pattern determination and microsporogenesis goes beyond a simple correlation with the type of cytokinesis or the way the cytoplasm is partitioned after each meiotic division.
Conclusion
This study of the diversity and evolution of microsporogenesis in angiosperms is the first large-scale overview of microsporogenesis that includes not only the type of cytokinesis but also information concerning intersporal wall formation and tetrad form. This comprehensive study allowed us to demonstrate clearly that the pathway associated with successive cytokinesis is restricted to wall formation mediated by centrifugally developing cell plates and tetragonal (or decussate, T-shaped, linear) tetrads, whereas much more flexibility (in terms of tetrad form and intersporal wall formation) can be found when cytokinesis is simultaneous (the production of only tetragonal tetrads is therefore not sufficient evidence that cytokinesis is successive). Our results suggest that the ancestral pathway for angiosperms, and likely for all seed plants, associated simultaneous cytokinesis with centripetal wall formation, thus resulting in a large diversity in tetrad forms that range from regular tetrahedral to tetragonal, including rhomboidal tetrads. The variability observed in the shape of the tetrad suggests the absence of direct selective pressures on this character, indicating that the production of the monoaperturate pollen type (the most common type in gymnosperms and basal angiosperms) can be achieved rather independently of the tetrad form. Conversely, the fact that the eudicots evolved toward an almost exclusive production of regular tetrahedral tetrads is an argument in favor of a major role of the tetrad form in the determination of the aperture pattern for tricolpate pollen grains, which may have played a key role in eudicot diversification (Furness and Rudall, 2004). Recurrent switches toward successive cytokinesis occurred among basal angiosperms (Furness et al., 2002), in the ancestor of all monocots and secondarily within the Asparagales (Furness and Rudall, 1999). Interestingly, the transitions toward the successive type result in a higher similarity of cytokinesis between the mitotic and meiotic cell division processes. These processes are dissimilar in most land plants in that no preprophase band is observed during sporogenesis and because during mitosis, karyokinesis is always followed by cytokinesis between the two sister nuclei achieved by a centrifugally developing cell plate (Brown and Lemmon, 1991; Smith, 1999). This latter feature is exactly what is observed during microsporogenesis when cytokinesis is successive, raising the question of which genes might be involved in these mechanisms. As yet, little is known about the genetic control of male meiotic divisions in plants. A few genes have been identified in Arabidopsis thaliana, such as SPOROCYTELESS, which is essential for sporocyte formation (Yang et al., 1999), TETRASPORE, and STUD, which are required for cytokinesis (Hülskamp et al., 1997; Spielman et al., 1997), and TAM, which is involved in the synchronization of cytokinesis after karyokinesis (Magnard et al., 2001). It would be interesting to further explore and compare the genetic bases of mitotic vs. meiotic division to address the question of whether the similarity between mitosis and successive meiosis results from independent recruitment of different genes or whether the same genes are implicated.
FOOTNOTES
1 The authors thank the various botanical gardens from which plant material was obtained: Jardin Botanique de la Ville de Paris (France), Conservatoire Botanique National de Brest (France), Parc Botanique de Launay (France), Royal Botanic Gardens Kew (UK), Kirstenbosch National Botanical Garden (South Africa), CBNB. The authors thank A. Forchioni for technical support and F. Jabbour for helpful discussions, the two reviewers for their helpful comments, and the IFR87 "La plante et son environnement" for financial support. 
5 Author for correspondence (e-mail: sophie.nadot{at}u-psud.fr)
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