| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
Corresponding author: Daniel Grimanelli, Department of Applied Biotechnology, CIMMYT APDO 6-641, 06600 México DF, México., dgrimanelli{at}cgiar.org (E-mail)
Communicating editor: J. BIRCHLER
 | ABSTRACT |
|---|
 TOP ABSTRACT MATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Some angiosperms reproduce by apomixis, a natural way of cloning through seeds. Apomictic plants bypass both meiosis and egg cell fertilization, producing progeny that are genetic replicas of the mother plant. In this report, we analyze reproductive development in Tripsacum dactyloides, an apomictic relative of maize, and in experimental apomictic hybrids between maize and Tripsacum. We show that apomictic reproduction is characterized by an alteration of developmental timing of both sporogenesis and early embryo development. The absence of female meiosis in apomictic Tripsacum results from an early termination of female meiosis. Similarily, parthenogenetic development of a maternal embryo in apomicts results from precocious induction of early embryogenesis events. We also show that male meiosis in apomicts is characterized by comparable asynchronous expression of developmental stages. Apomixis thus results in an array of possible phenotypes, including wild-type sexual development. Overall, our observations suggest that apomixis in Tripsacum is a heterochronic phenotype; i.e., it relies on a deregulation of the timing of reproductive events, rather than on the alteration of a specific component of the reproductive pathway.
SEXUAL reproduction in angiosperms occurs within a highly differentiated multicellular structure, the ovule. The formation of the female gametes within the ovules entails two consecutive steps: megasporogenesis (spore formation) and megagametogenesis (gamete formation). Megasporogenesis initiates with the formation of the megaspore mother cell (MMC), which undergoes meiosis. Meiosis results in the production of four megaspores, containing half the number of chromosomes of the sporophyte. In most angiosperms, three of the four spores degenerate, leaving a single functional megaspore. During megagametogenesis, the megaspore undergoes mitotic divisions, typically three rounds, producing a multicellular gametophyte (the embryo sac) containing the gamete (the egg cell). In the most common type of gametophyte development in plants (the Polygonum type), the mature gametophyte contains one single egg cell, a central cell, two synergids at the micropylar pole, and a variable number of antipodal cells at the chalazal pole.
In male reproductive organs (the anthers), all four products of meiosis survive. They divide and differentiate to produce the male gametophyte (the pollen grain), which contains two reproductive sperm cells, both of which are involved in the double fertilization of the female gametophyte. The fertilization of the egg cell by one of two sperm cells leads to the formation of the embryo, while the fertilization of the central cell by the second male sperm cell gives rise to the endosperm. The central cell contains two nuclei. The endosperm and the embryo therefore have different ploidy levels: 3x for the endosperm and 2x for the embryo.
Gametophytic apomixis (referred to hereafter as apomixis) is a process of asexual reproduction through seeds (
Apomixis has been intensively studied at the structural level (
Here, we tested these hypotheses by analyzing diplosporous apomictic development in Tripsacum dactyloides L., a wild relative of maize (Zea mays L.), and in hybrids between apomictic Tripsacum and sexual maize plants. Our analyses suggest a more complex picture: apomixis in Tripsacum and maize-Tripsacum hybrids is characterized by an alteration of the developmental timing of sporogenesis and early embryo development, rather than by gametogenesis. We further demonstrate that the precocious initiation of embryo development can occur regardless of meiotic reduction and thus is not a direct consequence of the absence of meiosis. We suggest that apomixis in Tripsacum is a typical heterochronic phenotype: it results from the temporal alteration of the orderly progression of the developmental subroutines that constitute the sexual pathway, but without disruption of the subroutines themselves.
| MATERIALS AND METHODS |
|---|
| TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Plant materials:
We used two maize inbred lines, CML135 and CML139, and hybrids (referred to herein as the H1 hybrid) between those two lines as controls for wild-type sexual development in maize. A diploid, sexual T. dactyloides plant, accession BT-FCM, was used as a reference for sexual development in Tripsacum. Four apomictic accessions (nos. 65-1234, 11-36, 61-664, and 112-1327) of tetraploid T. dactyloides were obtained from the CIMMYT germplasm bank (http://www.cimmyt.org). They have been previously characterized for their mode of reproduction (
Various generations of maize-Tripsacum hybrids and hybrid derivatives were obtained with Tripsacum accession 65-1234. Pedigrees and a precise description of their reproductive behavior can be found elsewhere (
Cytological characterization of male and female meiocytes:
Female and male meiocytes were collected at various stages before tassel and ear emergence, fixed in a mix of ethanol:chloroform:acetic acid (6:3:1) for 24 hr, and stored in 75% ethanol. For male meiocytes, we fixed individual anthers after dissection from the florets. Chromatin was stained with 20 µl of 1 mg/ml 4',6-diamidino-2-phenylindole (DAPI) in 1x PBS buffer.
For female meiocytes, entire developing ears were fixed. We sampled for each material a total of 12 ears representing different stages of development from MMC differentiation (ears 1.5 cm long) to mature embryo sacs. The ovules were dissected, positioned in a 96-well plate to reflect their position on the ear, and analyzed individually. A minimum of 12 ovules were analyzed per sample. Stages of ovule development were observed in half of the ovules through whole-mount cleared ovules, while chromosome configuration was analyzed using DAPI staining for the other half of the ovules. For DAPI staining, ovules were extruded from the ovaries, digested for 15–30 min using a mix of 5% cellulase and 1% pectolyase in 0.01 M citrate buffer, washed twice in water, and placed on a slide. They were gently squashed to separate the cells and stained with DAPI. Preparations were observed directly with epifluorescence on a Leitz Aristoplan microscope. Ovule clearing was performed using a 2.1:1 solution of benzyl-benzoate:dibutyl-phtalate clearing solution as previously described (
Ploidy levels of mature pollen grains were estimated using flow cytometry. Pollen grains were extruded from freshly harvested anthers and directly analyzed using the same protocol used for leaf tissues. For each sample, five replicates consisting of a bulk of 10 different anthers were analyzed using a PARTEC CAII flow cytometer. A diploid maize line (CML216) was used as a standard in all measurements. Five thousand nuclei were counted for each entry.
Immunofluorescence:
Anthers of the appropriate stages were placed into 2 ml of fixative solution [8% (v/v) paraformaldehyde] and PHEMS buffer (60 mM Pipes, 25 mM HEPES, 10 mM EGTA, 2 mM MgCl2, and 0.32 M sorbitol, pH 7.2) for 30 min, rinsed, and stored in PHEMS buffer. Meiocytes were extruded from the anthers in a drop of 1x PBS and embedded in polyacrylamide following
Embryo development:
Maize, Tripsacum, and maize-Tripsacum hybrid materials were used to visualize timing of embryo development with and without fertilization in apomictic and sexual materials. For each, female inflorescences were pollinated under controlled conditions using H1 as a pollen donor. Immature ears were collected at 0, 8, 12, and 24 hr and at 2, 4, and 5 days after pollination (DAP). Nonpollinated materials were also collected by covering flowers to avoid pollination and collecting at an equivalent estimated time based on the timing of silk emergence. The samples were embedded in paraffin, sectioned, and stained using standard procedures. Images were collected with a CCD camera. Image manipulation and editing was performed using the GraphicConverter software (lemkesoft.com). DNA fingerprinting of seedlings was performed using a nonradioactive amplified fragment length polymorphism (AFLP) protocol (
| RESULTS |
|---|
| TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Megasporogenesis and megagametogenesis in maize and sexual Tripsacum:
Megasporogenesis and megagametogenesis in maize, which follows the Polygonum type of gametophyte development, have been described in various publications (
|
In addition, we looked at the synchronization of MMC and the ovule development in individual ovaries and between ovaries on the same ear. In maize, timing of ovule development and meiosis are synchronized. On the ears, they followed a regular gradient, with the most advanced ovules being located at the bottom of the ear and the youngest cells at the top. At a given height on the ear, "rings" of ovaries presented both synchronized ovules and synchronized meiocytes. Hence, development stages of the meiocytes can be predicted from the stages of ovule development, and reciprocally. In Tripsacum, ears were smaller and contained a limited number of female flowers, 15–25 in our accessions. All ovules and meiocytes on a given ear were found at very similar stages of development throughout female reproductive development.
Megasporogenesis and megagametogenesis in apomictic Tripsacum:
Diplospory was analyzed in a single entry of T. dactyloides, accession no. 65-1234. Ovule growth followed a path similar to that observed in maize and sexual Tripsacum. Synchronized ovules were observed on the ears all the way from MMC differentiation to mature ovaries. Contrary to the ovules, however, meiocytes were not synchronized. Chromatin staining of meiocytes after MMC differentiation identified two classes of cells. The first class (half of the cells, Table 1) contained cells in interphase. The second class contained developing embryo sacs. Those could be differentiated by their size, shape, and the presence of a large central vacuole (Fig 2). Ears analyzed at later stages of ovule development were all found to contain synchronized ovules, but embryo sacs of various maturity. No aborted ovules were observed at that stage, indicating that asynchronous development does not result in developmental arrest. Although the observation of ovule development stages indicates that our sampling covered extensively the period following MMC differentiation, meiotic chromosomes were never observed.
|
|
Megasporogenesis in maize-Tripsacum hybrid derivatives:
We first estimated the frequency of embryos derived through diplospory in 38C clones. All visible embryos (252 out of a total of 267 flowers or 94%) were extracted from three mature ears and analyzed for mode of reproduction using flow cytometry. Overall, 98% of the embryos originated from unreduced gametes (fertilized or not). The remaining 2% originated from sexual reproduction.
Ovule clearing showed that, as in maize, ovule development was synchronized on the ear. Surprisingly, 
30% of the meiocytes extracted after MMC differentiation displayed meiotic chromosome configurations with DAPI staining (Table 1; Fig 2). Early meiotic stages, leptotene or zygotene, were observed. No sample later than pachytene was recorded. The remaining meiocytes at similar stages of ovule development were differentiated, uninucleate embryo sacs similar to those found in Tripsacum. Ears sampled later during development, corresponding to ovules in late prophase I or meiosis II in sexual materials, also showed asynchronous meiocyte development (Table 1): while a majority of the cells were embryo sacs at various stages of development, 26% displayed either mitotic-like prophase (showing neither the chromosome pairing nor the typical distribution of chromosomes and organelles that are characteristic of female meiosis I) or dyads of individualized cells (Fig 2F and Fig G, respectively). Chromosome counts indicate that both cells in the dyads contained 38 chromosomes, similar to the mother plant (Fig 2). Such genomic constitution, consisting of two maize genomes (2x = 20) and one haploid Tripsacum genome (x = 18) is highly unstable through meiosis, as shown elsewhere (
Kernel development in sexual and apomictic Tripsacum:
Mature unpollinated ovaries collected from sexual Tripsacum individuals showed seven-celled megagametophytes of the Polygonum type. After pollination, both the embryo and the endosperm followed developmental courses typical of those observed in maize. Most unpollinated ovaries collected at maturity from Tripsacum plants and apomictic maize-Tripsacum hybrids showed a single Polygonum-type megagametophyte. However, a major difference was the presence of globular pro-embryos in 26 out of 30 preparations that we observed (Fig 2). Most globular pro-embryos were located at the micropylar end between the central cell with unfused neighboring polar nuclei and intact synergid cells. Presence of the synergids and the central cell nuclei shows that the pro-embryos developed from the egg cell. Pro-embryos contained 8–32 cells, indicating that the embryo had completed up to five mitotic divisions. Concomitant embryonic development was also observed in other cell types of the megagametophytes such as antipodal or synergid cells (two and three megagametophytes, respectively). The four remaining unfertilized megagametophytes showed a typical Polygonum-type organization with a normal-appearing egg cell.
Further development of the megagametophytes was observed at various times with and without pollination. In the later case, no development was noted in both pro-embryos and central cells, and the megagametophytes finally collapsed. Discharge of the pollen tube into megagametophytes collected from pollinated flowers was observed 8 hr after pollination (HAP). Further endosperm development followed a course similar to that observed in reduced megagametophytes. The first division of the primary endosperm nucleus was noted 20 HAP and resulted in a coenocytic sac with nuclei having migrated peripherally 3 DAP (Fig 2). After a short lag period, coenocytic endosperms started to cellularize between 4 and 5 DAP.
Although the pro-embryos were formed prior to pollination, they appeared arrested in development for several DAP. Throughout a 5-DAP period, they showed signs of neither further cell division nor developmental differentiation. First evidences of reinitiation of embryogenic development were noted 5 days after pollination as a few embryos at the transition stage were observed. At 7 and 8 DAP, embryos had reinitiated development in the 35 megagametophytes we observed (Fig 2). No evidences for a similar resting stage were found in sexual Tripsacum.
Polyembryos associated with single endosperms were observed in four cases (Fig 2). Polyembryony was further characterized by determining DNA content and fingerprints of embryos obtained from 157 polyembryonic kernels (Fig 2). Most pairs (129 or 82%) were composed of maternal clones. Among the remaining ones, we found mixtures of maternal and nonmaternal embryos (19 or 12%) and pairs of genetically identical but nonmaternal embryos (9 or 6%).
Male meiosis in Tripsacum:
We estimated the proportion of reduced, aneuploid, and unreduced male gametophytes in both the sexual and apomictic accessions using flow cytometry. In both sexual diploid maize and sexual diploid Tripsacum samples, only reduced male gametophytes were detected using flow cytometry. Similarly, unreduced pollen grains or pollen grains with more than a 4x complement for meiotic products were not detected with flow cytometry in sexual tetraploid maize. In apomictic Tripsacum accessions, however, unreduced pollen grains or aneuploid pollen grains of high ploidy levels (close to and eventually higher than 4x) represented on average 25% of the mature male gametophyte. Since a lot of the aneuploid products likely did not reach maturity because of unbalanced chromosomal complements, this estimate probably undervalues the frequency of abnormal male meiosis in apomictic samples.
To further characterize pollen development in apomicts, we analyzed male meiosis in four different apomictic accessions, including accession 65-1234. At least 200 cells covering all meiotic stages were scored for each entry. Results were consistent in all four accessions. Microsporogenesis in apomictic Tripsacum is characterized by numerous abnormalities (Fig 3). The first and foremost peculiarity concerns the synchronization of meiocyte development within the anthers; while, in sexual maize and sexual Tripsacum, meiocytes within an anther are usually well synchronized, this is not the case in apomictic Tripsacum. During meiosis I, for example, cells could be found from leptotene to pachytene in a single anther.
|
Wild-type meiocytes, i.e., without noticeable defaults, were seldom observed (Table 2). Loose condensation of chromosomes was observed in 12% of the cells from diakinesis to anaphase. Most cells at metaphase (>80%) contained both univalents and chromosomes that failed to align to the metaphase plate (Fig 3A and Fig B). They still formed spindles that were similar to the wild-type meiocytes. Most of the unaligned chromosomes were not attached to the main spindle. Some of them created a local array of disorganized microtubules. In 8% of the meiocytes at metaphase, a marked asynchrony between chromosome behavior and cell division was observed. In those cells, cytokinesis took place during the meiotic prophase I. As observed in Fig 3C, cell division is near completion while the chromosomes are still aligned at the metaphase plate, and the meiotic spindle is fully formed. Defaults in cell division were also observed at later stages (Fig 3, D–F). In 32% of the meiocytes in meiosis II, cytokinesis was either independent of cell division (taking place before nuclear division) or misoriented.
|
Although virtually all cells reveal some defaults, there is no consistency in phenotype; individual cells might or might not present one or more of the above characteristics. Rather, male meiosis is apparently disturbed in numerous facultative ways, resulting in an array of possible phenotypes.
Pattern of histone phosphorylation during male meiosis:
An antibody that recognizes a ser10 phosphoepitope on histone H3 was used to monitor H3 phosphorylation during meiosis in both sexual and apomictic materials. Histone H3 phosphorylation has been reported to be an excellent marker of condensation for meiotic and mitotic chromosomes in maize (
We scored a minimum of 100 cells per entry at each stage mentioned hereafter. In both sexual maize and sexual Tripsacum, patterns of histone H3 (Fig 3G and Fig H) phosphorylation conformed to the published literature (55% of the male meiocytes in accession 65-1234, H3 phosphorylation was first observed before or during pachytene (Table 2). In those cells, it started with 8–13 initiation sites (average 11, calculated on the basis of 58 cells with clear signals at pachytene), the remaining chromosomes showing no phosphorylation signals. By diakinesis, >70% of the cells showed phosphorylation signals. After diakinesis, normal phosphorylation patterns were observed in all cells.
| DISCUSSION |
|---|
| TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Apomeiosis results from heterochronic termination of female meiosis:
In sexual Tripsacum as in sexual maize plants, ovule development and female gamete formation are synchronized; ovules at a particular time in organogenesis contain reproductive cells at predictable stages. Thus, meiocyte development in sexual and apomictic plants can be compared for similar developmental steps by monitoring ovule development. At stages of ovule development corresponding to early meiosis in sexual Tripsacum and maize plants, meiotic chromosomes were never observed in apomictic accessions. Instead, meiocytes were either in premeiotic interphase or already differentiated as immature uninucleate embryo sacs. These observations are consistent with the expected Antenaria type of diplospory in Tripsacum: the MMC totally skips meiosis and directly differentiates into a uninuclear embryo sac. The entire set of events taking place during wild-type sporogenesis is short circuited.
In contrast to apomictic Tripsacum, the modalities of apomeiosis in the 38C maize-Tripsacum derivatives varied significantly from cell to cell. The reasons for such plasticity are unclear. Nevertheless, our observations provide valuable details regarding the mechanisms of diplospory. Early stages of meiosis I, leptotene to pachytene, were observed in the 38C plants. However, the occurrence of meiosis in 38C was rare (<2% of the progeny). Because our analysis techniques are destructive, we could not observe the various stages of apomictic development on the same ear. Nonetheless, there is no evidence to indicate that the subsets that were used to evaluate early diplosporous stages and progeny types differed in any respect. Since our survey of the progeny types in 38C materials was almost exhaustive (94% of the flowers sampled), we assume that most of the cells that initiated meiosis produced unreduced gametes. A likely explanation can be found in cells observed later during development. Cells predicted in metaphase I on the basis of ovule development could be classified into two groups. The first one includes multinucleate embryo sacs. These likely arose from an Antenaria type of development. The second group, with a proportion similar to the cells initiating meiosis at an earlier stage (26%), includes cells in various mitotic configurations.
From those observations, we understand that most meiocytes initiating meiosis neither completed the process (reduced spores represent <2%) nor aborted (98% of the flowers produce unreduced egg cells). Rather, we propose that those cells revert to mitosis, thereby overturning their earlier commitment to meiosis. Under this hypothesis, diplospory in Tripsacum would affect early steps of megaspore formation, inducing a heterochronic exit from meiosis. In the extreme heterochronic phenotype, meiosis would be skipped entirely.
Similar processes have been reported in yeast: early meiotic cells can reenter a mitotic cell cycle when transferred from sporulation to growth medium (
We cannot speculate on the mechanisms inducing an exit from meiosis. However, our observations suggest that diplospory is not the result of altered meiotic functions. In particular, diplosporous plants conserved intact the potential for both male and female meiosis. Furthermore, diplospory in Tripsacum leads to the formation of functional gametes. Meiosis, however, is actively controlled by checkpoints (
According to a popular model, the early termination of sporogenesis results from an early induction of gametogenesis. Our observations point to a different model. In particular, we observed that the dyads observed at stage 2 (see Table 1) resulted from mitotic-like, rather than meiotic, first divisions. This indicates that the cells that failed the first meiotic division remained committed to sporogenesis, rather than to gametogenesis. Thus, termination of meiosis occurred independently of the initiation of gametogenesis. Altogether we therefore conclude that diplospory induced heterochronic exit from meiosis by affecting the developmental timing of sporogenesis.
Our observations also suggest an important difference between the aposporous and diplosporous types of development. In aposporous apomictic plants, a somatic cell from the nucellus differentiates into a spore and undergoes the postmeiotic events of gametogenesis. This implies that the first consequence of apospory is a shift in cell fate within the nucellus (
Parthenogenesis results from heterochronic induction of early embryogenesis:
In sexual plants, seed development relies upon double fertilization. Here, we show that in apomictic Tripsacum, pro-embryos progress up to five divisions prior to fertilization. The presence of pro-embryos in Tripsacum has been reported previously (
This observation suggests that the embryo in apomicts passes through two clearly different stages of development, separated by a crucial transition point and taking place after three to five divisions. The first stage, represented by the pro-embryo, is independent of fertilization. Rather, pro-embryo development is part of the formation of the mature embryo sac. It is therefore fully under maternal control.
Recent reports have shown that early seed development in Arabidopsis is largely under maternal control and that most male-derived alleles are silent during the first divisions of the zygote (
What induces precocious embryo development in apomicts is unclear. It is often mentioned in the literature that parthenogenesis might be a pleiotropic consequence of apomeiosis (
Male meiosis reveals unique aspects of apomixis in Tripsacum:
It is generally accepted that diplospory is a female-specific trait. Here, however, we showed that diplospory likely affects early stages of female meiosis. Furthermore, our observations also suggest that in Tripsacum, the progression of both male and female meiosis is affected in similar ways. As such, microsporogenesis, which is much more exploitable for cellular characterization, might provide a useful source of indirect information regarding the cellular processes involved in apomeiosis.
Flow cytometry indicates that meiosis in four distinct apomictic Tripsacum accessions results in a large proportion of unreduced or aneuploid male gametophytes, together with reduced pollen grains. Although virtually all male meiocytes in apomictic Tripsacum present abnormal development, we could not identify any specific phenotype. Rather, male meiosis is seemingly altered in numerous, facultative ways. In all instances, those alterations relate to the timing of the initiation of cellular events. Not all the phenotypic abnormalities observed in male meiocytes are necessarily a primary effect of diplospory. Apomixis plants can certainly accumulate mutations in the male function without significantly altering their overall fitness. Nevertheless, the defects reported here are unlikely to result exclusively from accumulation of unrelated mutations. A notable feature of male meiosis in apomictic Tripsacum is the absence of clear-cut phenotypes. This reflects a relaxed selection of the progression of meiosis rather than altered meiotic functions, a phenomenon that is a hallmark of female sporogenesis in apomictic Tripsacum. Three processes are particularly illustrative. The first one is the loss of synchronization between cells within the anthers. The second one is the loss of synchronization between cell division and chromosome movements within individual meiocytes. This occurs at several stages, including metaphase I and prophase II, and shows that, in apomictic Tripsacum, developmental programs (such as cytokinesis and nuclear division) can be superimposed on each other, leading to the precocious termination of the earlier of the two programs. This is very similar to what was observed for the termination of meiosis in female meiocytes in apomicts.
The third process is the pattern of histone H3 phosphorylation. In apomicts, histone H3 phosphorylation occurs much earlier than in sexual materials, illustrating the heterochronic expression of pieces of the meiotic process. Interestingly, not all chromosomes show synchronized phosphorylation. The number of initiation sites is limited to a subset of the chromosomes, an observation unique to apomicts. This supports the "genome asynchrony" model for the regulation of apomixis (
Conclusion: apomixis results from a global deregulation of sexual developmental programs:
During sexual development, reproductive organs and cells within the reproductive organs undergo predictable and synchronized temporal and spatial changes. Not so in apomictic Tripsacum, where the progression through spore, gamete, and embryo formation suffers alterations as compared to the sexual forms. Our current model is summarized in Fig 4. Our data indicate that apomixis in Tripsacum causes a highly plastic heterochronic phenotype, resulting from a deregulation of the developmental timing of sporogenesis and early embryogenesis. Apomixis in Tripsacum is built of blocks of the sexual development pathways, whose expression is altered in time. It depends on an alteration of the orderly progression of developmental subroutines, rather than on the establishment of a new function. How such a model might fit with the current genetic evidence, which implies a limited number of mutant genes, remains an open question. Genetic screens for regulators of the developmental timing of female reproduction might shed some light on this fascinating problem.
|
| FOOTNOTES |
|---|
2 Present address: CINVESTAV-Irapuato, Departamento de Ingeniería Genética, CP 36 500, Irapuato GTO, Mexico. 
| ACKNOWLEDGMENTS |
|---|
Thanks go to Marc Albertsen, Andreas Betzner, Dave Hoisington, Jean Philippe Vielle-Calzada, Stewart Gillmor, Ueli Grossniklaus, and an anonymous reviewer for stimulating discussions on apomixis. This work is funded by the Institut de Recherche pour le Développement, Pioneer Hi-Bred, Syngenta Seeds, and Group Limagrain through a joint Apomixis Research Consortium.
Manuscript received April 11, 2003; Accepted for publication July 23, 2003.
| LITERATURE CITED |
|---|
| TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
ASKER, S., and L. JERLING, 1992 Apomixis in Plants. CRC Press, Boca Raton, FL.
BANTIN, J., F. MATZK, and T. DRESSELHAUS, 2001 Tripsacum dactyloides (Poaceae): a natural model system to study parthenogenesis. Sex. Plant Reprod. 14:219-226.
BAROUX, C., R. BLANVILLAIN, and P. GALLOIS, 2001 Paternally inherited transgenes are down-regulated but retain low activity during early embryogenesis in Arabidopsis. FEBS Lett. 509:11-16.[Medline]
BASS, H. W., W. F. MARSHALL, J. W. SEDAT, D. A. AGARD, and W. Z. CANDE, 1997 Telomeres cluster de novo before the initiation of synapsis: a three-dimensional spatial analysis of telomere positions before and during meiotic prophase. J. Cell Biol. 137:5-18.
CARMAN, J. G., 1997 Asynchronous expression of duplicate genes in angiosperms may cause apomixis, bispory, tetraspory, and polyembryony. Biol. J. Linn. Soc. 61:51-94.
FARQUHARSON, L. I., 1955 Apomixis and polyembryony in Tripsacum dactyloides. Am. J. Bot. 42:737-743.
GOLUBOVSKAYA, I., N. A. AVALKINA, and W. F. SHERIDAN, 1992 Effects of several meiotic mutations on female meiosis in maize. Dev. Genet. 18:411-424.
GRIMANELLI, D., O. LEBLANC, E. ESPINOSA, E. PEROTTI, and D. GONZALEZ DE LEON et al., 1998 Non-Mendelian transmission of apomixis in maize-Tripsacum hybrids caused by a transmission ratio distortion. Heredity 80:40-47.
GRIMANELLI, D., O. LEBLANC, E. PEROTTI, and U. GROSSNIKLAUS, 2001 Developmental genetics of gametophytic apomixis. Trends Genet. 17:597-604.[Medline]
GROSSNIKLAUS, U., G. A. NOGLER, and P. J. VAN DIJK, 2001 How to avoid sex: the genetic control of gametophytic apomixis. Plant Cell 13:1491-1498.
HOISINGTON, D., M. KHAIRALLAH and D. GONZÁLEZ-DE-LEÓN, 1994 Laboratory Protocols: CIMMYT Applied Molecular Genetics Laboratory, Ed. 2. CIMMYT, México D. F., México.
HONIGBERG, S. M. and R. E. ESPOSITO, 1994 Reversal of cell determination in yeast meiosis: postcommitment arrest allows return to mitotic growth. Proc. Natl. Acad. Sci. USA 91:6559-6563.
HUANG, B.-Q. and W. F. SHERIDAN, 1996 Embryo sac development in the maize indeterminate gametophyte1 mutant: abnormal nuclear behavior and defective microtubule organization. Plant Cell 8:1391-1407.[Abstract]
KASZAS, E. and W. Z. CANDE, 2000 Phosphorylation of histone H3 is correlated with changes in the maintenance of sister chromatid cohesion during meiosis in maize, rather than the condensation of the chromatin. J. Cell Sci. 113:3217-3226.[Abstract]
KOLTUNOW, A. M., 1993 Apomixis: embryo sacs and embryos formed without meiosis or fertilization in ovules. Plant Cell 5:1425-1437.
LEBLANC, O., M. D. PEEL, J. G. CARMAN, and Y. SAVIDAN, 1995 Megasporogenesis and megagametogenesis in several Tripsacum species (Poaceae). Am. J. Bot. 82:57-63.
LEBLANC, O., D. GRIMANELLI, N. ISLAM-FARIDI, J. BERTHAUD, and Y. SAVIDAN, 1996 Reproductive behavior in maize-Tripsacum polyhaploid plants: implications for the transfer of apomixis into maize. J. Hered. 87:108-111.
MCCARROLL, R. M. and R. E. ESPOSITO, 1994 SPO13 negatively regulates the progression of mitotic and meiotic nuclear division in Saccharomyces cerevisiae. Genetics 138:47-60.[Abstract]
NOGLER, G. A., 1984 Gametophytic apomixis, pp. 475–518 in Embryology of Angiosperms, edited by B. M. JOHRI. Springer-Verlag, Berlin.
NOYES, R. D. and L. H. RIESEBERG, 2000 Two independent loci control agamospermy (apomixis) in the triploid flowering plant Erigeron annuus. Genetics 155:379-390.
ROEDER, G. S. and J. M. BAILIS, 2000 The pachytene checkpoint. Trends Genet. 16:395-403.[Medline]
RUSSELL, S. D., 1978 Fine structure of megagametophyte development in Zea mays.. Can. J. Bot. 57:1093-1110.
SAVIDAN, Y., 2000 Apomixis: genetics and breeding, pp. 13–86 in Plant Breeding Reviews, edited by J. JANICK. John Wiley & Sons, New York.
SPRINGER, P. S., D. R. HOLDING, A. GROOVER, C. YORDAN, and R. A. MARTIENSSEN, 2000 The essential Mcm7 protein PROLIFERA is localized to the nucleus of dividing cells during the G(1) phase and is required maternally for early Arabidopsis development. Development 127:1815-1822.[Abstract]
TUCKER, M. R., A. C. ARAUJO, N. A. PAECH, V. HECHT, and E. D. SCHMIDT et al., 2003 Sexual and apomictic reproduction in Hieracium subgenus Pilosella are closely interrelated developmental pathways. Plant Cell 15:1524-1537.
VIELLE-CALZADA, J. P., R. BASKAR, and U. GROSSNIKLAUS, 2000 Delayed activation of the paternal genome during seed development. Nature 404:91-94.[Medline]
WEIJERS, D., N. GELDNER, R. OFFRINGA, and G. JURGENS, 2001 Seed development: early paternal gene activity in Arabidopsis. Nature 414:709-710.[Medline]
This article has been cited by other articles:
 |
|
 |
|
  D. Grimanelli, E. Perotti, J. Ramirez, and O. Leblanc Timing of the Maternal-to-Zygotic Transition during Early Seed Development in Maize PLANT CELL, April 1, 2005; 17(4): 1061 - 1072. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
