Whole Genome Approaches to Identify Genes Involved in Early Meiosis

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77 BMC Genomics BioMed Central

Research article Open Access Microarray expression analysis of meiosis and microsporogenesis in hexaploid bread wheat Wayne Crismani1, Ute Baumann2, Tim Sutton2, Neil Shirley2, Tracie Webster3, German Spangenberg3, Peter Langridge2 and Jason A Able*1

Address: 1Molecular Plant Breeding Cooperative Research Centre, School of Agriculture, Food and Wine, The University of Adelaide, Waite Campus, PMB1, Glen Osmond, South Australia, 5064, Australia, 2Australian Centre for Plant Functional Genomics, School of Agriculture, Food and Wine, The University of Adelaide, Waite Campus, PMB1, Glen Osmond, South Australia, 5064, Australia and 3Molecular Plant Breeding Cooperative Research Centre and Australian Centre for Plant Functional Genomics, Victorian AgriBiosciences Centre, La Trobe University, 1 Park Drive, Bundoora, Victoria, 3083, Australia Email: Wayne Crismani - [email protected]; Ute Baumann - [email protected]; Tim Sutton - [email protected]; Neil Shirley - [email protected]; Tracie Webster - [email protected]; German Spangenberg - [email protected]; Peter Langridge - [email protected]; Jason A Able* - [email protected] * Corresponding author

Published: 19 October 2006 Received: 12 September 2006 Accepted: 19 October 2006 BMC Genomics 2006, 7:267 doi:10.1186/1471-2164-7-267 This article is available from: http://www.biomedcentral.com/1471-2164/7/267 © 2006 Crismani et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract Background: Our understanding of the mechanisms that govern the cellular process of meiosis is limited in higher plants with polyploid genomes. Bread wheat is an allohexaploid that behaves as a diploid during meiosis. Chromosome pairing is restricted to homologous chromosomes despite the presence of homoeologues in the nucleus. The importance of wheat as a crop and the extensive use of wild wheat relatives in breeding programs has prompted many years of cytogenetic and genetic research to develop an understanding of the control of chromosome pairing and recombination. The rapid advance of biochemical and molecular information on meiosis in model organisms such as yeast provides new opportunities to investigate the molecular basis of chromosome pairing control in wheat. However, building the link between the model and wheat requires points of data contact. Results: We report here a large-scale transcriptomics study using the Affymetrix wheat GeneChip® aimed at providing this link between wheat and model systems and at identifying early meiotic genes. Analysis of the microarray data identified 1,350 transcripts temporally-regulated during the early stages of meiosis. Expression profiles with annotated transcript functions including chromatin condensation, synaptonemal complex formation, recombination and fertility were identified. From the 1,350 transcripts, 30 displayed at least an eight-fold expression change between and including pre-meiosis and telophase II, with more than 50% of these having no similarities to known sequences in NCBI and TIGR databases. Conclusion: This resource is now available to support research into the molecular basis of pairing and recombination control in the complex polyploid, wheat.

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Background While functional studies of individual genes have been Bread wheat (Triticum aestivum L.) is an allohexaploid (2n useful for advancing our knowledge of meiosis, very few = 6x = 42) containing three related genomes: A, B and D, resources are available to examine whole genome expres- with significant conservation of gene order between the sion changes during meiotic development. A broad chromosomes of the respective genomes. Early mapping resource base will be important to help identify conserved studies including those conducted by Chao et al. [1] using processes between organisms, and conversely, highlight RFLPs to map markers on chromosome group 7 con- processes that have diverged. Microarray studies have pro- firmed strong conservation of gene order between chro- vided valuable data on meiosis and related cellular proc- mosomes of each genome. Indeed, this conservation is esses in several species. An early study in Saccharomyces also seen when comparing wheat with other grasses. cerevisiae used a microarray chip with 97% of the then While several papers have been published reporting syn- known budding yeast genes [6], which increased the teny between the Poaceae genomes at the macro level number of known meiotically-regulated genes from [2,3], microsynteny appears to be perturbed frequently approximately 150 to over 1,000. A more recent experi- [4,5]. The current comparative genomics model reported ment with budding yeast compared the meiotic transcrip- by Devos [3] segregates nine major monocotyledonous tomes of two strains with different sporulation efficiencies genomes into 25 'rice linkage blocks' and provides a valu- and identified approximately 1,600 meiotically-regulated able base for gene discovery and genome structural analy- genes in each strain with a 60% overlap between the two sis in grass species leading out from the sequenced rice strains [7]. While these two examples are yeast specific, genome. other model organisms have also been used to study meiosis with microarray technology, including fruit flies (Dro- While comparative genomics has enabled the identifica- sophila melanogaster), mice (Mus musculus), nematodes tion of putative orthologues in many cereals, there are (Caenorhabiditis elegans) and rats (Rattus rattus) [8-11]. processes or characteristics that are either species specific, such as quality, or for which wheat provides a good The current study provides information that links to the model, such as the control of chromosome pairing during transcript profiling work conducted in yeast and animal meiosis. During meiosis, DNA undergoes a round of rep- systems and to the extensive cytological and genetic data lication, chromatin is condensed and the genetic content for wheat to provide a view of meiosis in a complex poly- is halved twice after two rounds of chromosome segrega- ploid and one of the world's most important agricultural tion and cell division. Classical cytogenetic techniques crops. Using the Affymetrix GeneChip® Wheat Genome suggest that the fundamental events and processes of mei- Array, which contains 61,127 probe sets (55,052 tran- osis are conserved amongst higher eukaryotes. The pro- scripts) (Affymetrix), 1,350 transcripts were found to be duction of viable gametes at the conclusion of meiosis expressed across a sub-staged meiotic time series of whole requires completion of several critical processes during wheat anthers. Four hundred and sixty seven have no prophase I that include chromosome pairing, synapsis detectable similarities to entries in sequence databases. and recombination. While there have been extensive studies on the duration and timing of meiosis in bread wheat [12-15] and also on During meiosis in bread wheat, strict regulation of chromatin condensation and chromosome pairing [16- homologous chromosome pairing is maintained, despite 18], the transcript in silico research presented here the presence of homoeologous chromosomes. This main- advances our limited understanding of meiosis at the tains the stability of the complex wheat genome but is also molecular level and complements the previous in planta a limitation in utilizing the extensive variation available studies cited. in wild relatives of wheat. Several hundred wild grasses can be crossed to wheat but introgression of desirable alle- Results and Discussion les from these species is dependent upon the induction of The basic aim of the work outlined here was to develop a pairing and recombination with the wheat chromosomes. view of gene expression over the various stages of meiosis Several genes, particularly Ph1, are known to block or in wheat. The resulting data set helps define the wheat enhance homoeologous pairing; with removal of this meiome (meiotic transcriptome) and will provide a key locus shown to induce novel pairing and recombinational resource for work aimed at explaining the control of mei- behaviour. An understanding and ability to modify the osis and chromosome pairing in a complex polyploid rel- mechanisms that control pairing, synaptonemal complex ative to diploid plant, animal and yeast systems. formation and recombination would be of great benefit to crop improvement programs. Such information would Comparison of tissue expression profiles also enhance our understanding of complex polyploidy There are two key components of the experimental sys- genomes and factors influencing fertility. tem. First, whole anthers were used for preparing the RNAs. The meiocytes themselves form a major proportion

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of the tissues in the anthers but RNA from other cell types, (LP); PM with diplotene-anaphase I (DA); PM with telo- notably epidermal cells and tapetum, will be included in phase I-telophase II (TT); LP with DA; LP with TT and DA the extracts and will contribute to the results. Therefore, with TT (p values = 0.05) (Figure 1). This resulted in the the data represents gene expression from a number of dif- classification of transcripts from 1,350 non-redundant ferent cell types with meiocytes as the major constituent. genes as being meiotically-regulated of which 467 had no annotation (Figure 2). A similar strategy was used by Sch- The second component is the Affymetrix wheat Gene- lecht and colleagues [10] with a rat data set to examine Chip®. This is a 'discovery' chip and is not representative both meiosis and gametogenesis. The rat analysis resulted of the complete wheat genome nor does it allow differen- in the identification of 1,268 diverse meiotic transcripts tiation between genes expressed from the three wheat from a total of 11,955. genomes. Further, many of the sequences used to design the chip were not of high quality. Therefore, data gener- When compared to the 55,000 relevant probe sets on the ated from this chip must be carefully checked and key current wheat GeneChip®, the 1,350 meiotically-regulated results confirmed using alternative expression analysis transcripts represent only 2.45%. Thirty prominent pro- methods. In addition, it is important to note that at the files within the 1,350 meiotically-regulated transcripts time the wheat GeneChip® was designed, wheat meiotic showed at least an eight-fold expression change between floret cDNA and cDNA from anthers undergoing meiosis combinations of PM, LP, DA and TT. Of these 30 tran- represented approximately 6% of the total representations scripts, no similarities to any database entries currently on available in the wheat EST database. Therefore, the wheat record (August 2006) could be found for 16. Conse- GeneChip® is assumed to provide a good representation of quently, these represent a source of new and potentially meiotic expressed genes. wheat meiosis-specific transcripts. Seven of the 30 transcripts significantly change in level of expression during Scatter plots illustrated the similarity of replicates, and the the first three meiotic time points investigated in this broad relationship of the expression profiles from pre- study (Figure 3). It is during these stages where events meiosis through to the tetrad stage (Figure 1). However, including chromosome pairing, synapsis and homolo- marked differences were apparent in the expression pro- gous recombination occur. The temporal expression of files of both immature pollen and mature anthers when the genes encoding these transcripts at the time points compared to each other and the meiotic-specific sub- where homologous recombination occurs make them stages; pre-meiosis through to tetrads. Given that both of particularly interesting targets for further work aimed at these tissues and the regulation of gene expression during investigating homologous pairing and recombination. pollen development is complex, this level of variance is not surprising. It has been shown in several plants includ- The mature anthers (MAN) accounted for the majority of ing tomato (Lycopersicon esculentum) and maize (Zea mays) variability detected (73%) between transcript profiles that up to 70% of plant genes are expressed post-meioti- across the developmental stages. This is consistent with cally [19,20]. A study of the barley transcriptome also work on pollen development in Tradescantia and maize. found that anthers were the most complex of tissues [21]. Pollen germination and pollen tube growth are two proc- The results presented here reflect these findings with 67% esses that carry a significant metabolic cost, since it of transcripts expressed in tetrads, immature pollen and/ involves storage of mRNA and other organic molecules or mature anthers (RMA average signal intensity > 5). [22]. Previous studies of pollen development have typi- cally used inhibitors of transcription and translation to Gene filtration, identification and analysis of meiotically- show that mRNAs are produced during pollen maturation regulated transcripts and stored for use during pollen germination [for reviews The Affymetrix wheat GeneChip® contained 61,127 probe see [23,24]]. Further, many of the protein products of sets, which was reduced to 55,000 upon the removal of these genes are already present in mature pollen prior to control, reporter, duplicate and 'rogue' probe sets (see germination [25-27]. Methods – Microarray analysis). The majority of the available annotations for the probe sets are based on homolo- Transcript expression during pollen maturation is gener- gies to genes from organisms other than wheat. This was ally defined as either early or late, with early transcripts due to the lack of sequence information, characterised present in microspores subsequently down regulated genes and their protein products for wheat. before pollen maturation, while late transcripts are produced and accumulated after pollen mitosis I [reviewed in T-tests between expression levels at different stages of mei- [28]]. In situ studies from tomato and maize suggest that osis were used to identify genes showing regulation of many of the late genes are the product of the vegetative expression during meiosis. The comparisons made were cell [29,30]. Studies in both Tradescantia and maize have as follows: pre-meiosis (PM) with leptotene-pachytene

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anotherFigureScatter plot1 and statistical analysis comparing all seven stages investigated with the wheat Affymetrix GeneChip® to one Scatter plot and statistical analysis comparing all seven stages investigated with the wheat Affymetrix Gene- Chip® to one another. PM = pre-meiosis; LP = leptotene to pachytene; DA = diplotene to anaphase I; TT = telophase I to telophase II; T = tetrads; IP = immature pollen; MAN = mature anthers. All values in the figure represent the number of transcripts with corrected p-values 0.05 from t-tests performed between the two tissues of interest. The orange shading represents the pooled stages from where the 1,350 non-redundant meiotically-regulated transcripts were identified.

revealed that about 10% of mRNAs stored in mature pol- Expression analysis in the developing wheat anther len grains are pollen-specific [31,32]. The complexity of the anther tissues used in this study meant that interpretation of the data required a consider- Over the seven stages investigated in this study, 38,242 ation of developmental changes that were occurring in transcripts were differentially expressed in mature anthers anther cells other than just the meiocytes. To obtain a when compared to the first four stages of the meiotic time view of gene expression changes that may be indicative of course (p 0.05 between PM v MAN, LP v MAN, DA v the meiotic process and also general developmental shifts, MAN and TT v MAN). Similarly, when immature pollen ten biological categories of potential significance were (IP) was compared to the four meiotic stages, considera- used to group members of the 1,350 diverse transcripts ble variation was still detected with 9,385 transcripts found to show variable expression (see Methods – Micro- showing differential expression. array analysis). These groups covered genes likely to be involved in tissue growth and differentiation such as

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FigureFiltration 2 process used for Affymetrix wheat GeneChip® data Filtration process used for Affymetrix wheat GeneChip® data. The controls and 'rogue' probe sets were removed from the data prior to filtration. Meiotically-regulated transcripts were then identified using t-tests, with NCBI database annotations retrieved for the remaining transcripts where available (E-value < e-10).

those related to hormone regulation, signal transduction division and ribosomal categories, inferring that the and development, as well genes involved in metabolic mRNA of these candidates is down-regulated in mature process. 146 probe sets fell into one of ten categories (Fig- anthers. While not as significant, the transcription factors, ure 4). organelle activity, signal transduction, lipid metabolism, development and protein metabolism categories also dis- During the first five meiotic stages used in this study, the played this downward trend as the anther matured. This majority of the categories showed no significant increase decline is occurring as the pollen matures and reflects the or decrease in the level of expression, indicating a degree shutting down of cell division, expansion and differentia- of transcriptional stability in the anthers over these stages tion. of development. However, there were more pronounced effects when comparing the mature anther stage across all Meiotic clusters 10 functional categories. In general, all 10 categories Hierarchical clustering showed decreased levels of expression during this stage of Hierarchical clustering of the 1,350 meiotically-regulated development when compared to the other tissues investi- transcripts was performed to identify common gene gated. This trend is particularly evident in the meiosis/cell expression patterns (Figure 5). This revealed two clusters

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14 Meiosis/cell division (41) Organelle activity (15) 6 6

4 4 12 2 2

0 0 10 -2 -2 -4

-4 -6 8 -8 -6 PM LP DA TT T IP MAN PM LP DA TT T IP MAN

6 Transcription factors (18) Secondary metabolism (10) 4 8

Log base 2 expression 6 2 4 4 2 0

-2 -2 2 -4 PM LP DA TT -4 -6

Meiotic time points -6 -8 PM LP DA TT T IP MAN PM LP DA TT T IP MAN Ribosomal (8) Hormone regulation (9) FigureTranscriptslevel between 3 with and at including least an eight-foldpre-meiosis change to telophase in expression II 2 6 Transcripts with at least an eight-fold change in 1 4 expression level between and including pre-meiosis 0 2 to telophase II. Black = TaAffx.9800.1.S1_at; red = -1 0 TaAffx.60258.2.S1_s_at; light green = Ta.10020.1.S1_at; blue -2 -2 = Ta.6922.1.S1_at; pink = TaAffx.38162.1.S1_at; dark green = Ta.16669.1.S1_x_at; and grey = Ta.6831.1.S1_at. PM, LP, DA -3 -4 -4 -6 and TT are as described in Figure 1. PM LP DA TT T IP MAN PM LP DA TT T IP MAN Signal transduction (15) Lipid metabolism (11) 3 4

2 2 1

0 with 88 and 50 transcripts (indicated by I and II on Figure 0 5) that were expressed at low levels throughout pre-meio- -1 -2 -2 sis to immature pollen, only to then rise sharply at the -3 -4 onset of mature anther development (fold changes of -4 -5 -6 12.91 and 3.12, respectively). Within these two clusters, PM LP DA TT T IP MAN PM LP DA TT T IP MAN there were a number of transcripts present with known Development (12) Protein metabolism (7) annotations to genes that have roles in flower develop- 4 4 ment. One such candidate is the GRAB2 protein [33], 2 2 which contains a NAM (no apical meristem) domain. 0 0

NAM domains are part of the NAC domain family [34], -2 -2 which have been shown to have roles in cell division and -4 -4 cell expansion in floral organs, as well as determining the -6 -6 positions of meristems and primordia [35]. Another iden- PM LP DA TT T IP MAN PM LP DA TT T IP MAN tified transcript, NEC1, has been reported to have a role in FunctionaldevelopingFigure 4 classificationswheat anther and expression analysis from the the opening of anthers in petunia (Petunia hybrida) [36]. Functional classifications and expression analysis from the developing wheat anther. Transcripts were In addition to these flowering candidates, two PIP1 pooled into categories based upon their annotations and hav- aquaporin transcripts that have previously been isolated ing satisfied the following criteria: an E-value < e-30, a from wheat were identified. One could speculate that the sequence length > 250 bp and their cross-hybridizing status up-regulation of aquaporins during pollen maturation (based on the Affymetrix designation). The data for each helps prevent damage to reproductive structures. Previous functional category is represented as log base 2, RMA nor- work suggests that the products of this gene family help malized values that were centered on the average of the pre- meiosis (PM) value. Representations (n) assigned to each prevent chilling injury [37]. Although other annotated functional category are indicated in brackets. candidates were identified from these two clusters, approximately 53% of the transcripts showed no similarity to any known genes or proteins in the public databases (August 2006). An investigation of the roles of these unknown transcripts is likely to be useful in clarifying the developmental process involved in pollen maturation in

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PM LP DA TT T IP MAN III IV

6 2.0 4 III IV V 4 1.5 2 1.0 2

0.5 0 0 0.0 -2 -2 -0.5

-4 -1.0 -4 -6 -1.5

-8 -2.0 -6 PM LP DA TT T IP MAN PM LP DA TT T IP MAN PM LP DA TT T IP MAN

HierarchicalFigure 5 clustering of 1,350 meiotically-regulated transcripts Hierarchical clustering of 1,350 meiotically-regulated transcripts. The expression profiles of 1,350 transcripts (rows) were grouped across seven staged anthers (columns); pre-meiosis (PM), leptotene to pachytene (LP), diplotene to anaphase I (DA), telophase I to telophase II (TT), tetrads (T), immature pollen (IP) and mature anthers (MAN) (averages shown). Clusters of interest (described in text) are highlighted in blue and labelled I and II (pollen clusters); III, IV and V (meiotic clusters). The Y- axis for cluster groups III, IV and V is centered, log base 2, RMA normalized values.

wheat and other cereals. In particular, these genes are tion. Investigation of other genes in this group may pro- expressed shortly before full pollen maturity and dehis- vide valuable targets for general stress or desiccation cence. As the anthers used to prepare this RNA were still tolerance. green, at this stage there will be genes likely to be involved in preparing the pollen for release. This is consistent with Although the meiotic stages examined in this study could the putative role for the PIP genes in desiccation protec- have been more tightly defined (for example, leptotene

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could have been separated from pachytene), the timing ing the other two cluster groups (indicated by IV and V on and collection of such specific events during wheat meio- Figure 5), many transcripts were identified that have sis would not have guaranteed producing improved reso- already been reported to have roles in processes that occur lution. While Chu and colleagues [6] and Primig et al. [7] during early meiosis. Not only were transcripts that had divided their meiotic profiles into seven different catego- significant similarities to cell cycle proteins, kinesin- ries, these experiments used yeast, where synchronization related proteins and chromomethylases identified but and identification of specific individual meiotic stages is candidates implicated in chromosome pairing, synapsis simple. The meiotic time series used here is significantly and recombination were also represented. more detailed than those examined in other plant systems. Meiosis I and II in bread wheat anthers is completed To gain insight into the functional roles of genes identi- within 24 hours, with prophase I (which includes lepto- fied in these three clusters a similar strategy to that of tene, zygotene, pachytene, diplotene and diakinesis) tak- Iguchi and colleagues [38] was used, whereby transcripts ing 17 hours [14]. In contrast to other grasses, this is one were assigned to a biological category based on annotated of the most rapid to complete meiosis with rye (Secale functions. In cluster groups III, IV and V, approximately cereale) taking 51 hours and barley (Hordeum vulgare) tak- 40% of the 350 transcripts (pooled value from the three ing 39 hours [15]. This is partially explained by Bennett clusters) were either functionally not annotated or novel and Smith [14] who showed that in wheat, rye and Triti- (with no database matches returned) (Table 1). While the cale the duration of meiosis decreases as the ploidy level classifications of the 350 transcripts ranged from func- increases. tional categories as diverse as abiotic stress-related and secondary metabolism, a reasonable proportion (17%) Besides cluster groups I and II previously described, at represented unambiguous meiotic and/or cell division least three clusters (indicated by III, IV and V on Figure 5) candidates (Table 1). These transcripts were assigned to a appeared to be meiotically-regulated, suggesting that mei- specific meiotic and/or cell division category based on otic genes undergo subtle changes in expression, rather their annotation (Figure 6). Transcripts showing signifi- than sharp increased or decreased bursts of expression. cant database matches to histones, cell cycle and cytoskel- Possible reasons accounting for these observations etal candidates isolated from other organisms, as well as include; 1) there may not be a large number of genes chromosome-associated, recombination and mismatch exclusively involved in meiosis, irrespective of the repair genes were all identified. number of genes within the organism's genome; 2) meiosis classifications are largely based on cytological observations and may not reflect what is occurring at the transcript level, and 3) the 'dilution effect' of other tissues Table 1: Functional classifications for 350 meiotically-regulated present in wheat anthers. It should be noted that during transcripts. meiosis, chromatin is heavily condensed and this may Category Representations (%) pose limitations for the transcriptional machinery of the cell. Consequently, the expectation would be for gene Meiosis/cell division 60 (17.1) expression to be restricted to genes essential to the meiotic Cellular metabolism 24 (6.86) process. Transcripts required for other functions, such as Transcription factors and DNA binding 18 (5.14) general cell metabolism, would most effectively be pro- Ribosomal 15 (4.29) vided prior to the onset of meiotic condensation. Biotic stress-related 12 (3.43) Membrane transport 12 (3.43) Signal transduction 10 (2.86) Of the meiotically-regulated clusters identified, one clus- RNA processing 10 (2.86) ter contained only 15 transcripts, while the other two con- Development 8 (2.29) tained 48 and 287 transcripts (indicated on Figure 5 by III, Organelle activity 8 (2.29) IV and V respectively). The cluster of 15 transcripts (III) Secondary metabolism 7 (2.00) showed enhanced expression during the latter stages of Hormone regulation 5 (1.43) meiosis I. Consequently, these genes may be involved in Abiotic stress-related 5 (1.43) Lipid metabolism 4 (1.14) the latter stages of meiosis or the early stages of pollen Protein metabolism 4 (1.14) maturation. While 33% of these transcripts showed no Protein transport 4 (1.14) similarity to any known sequences in the public databases Protein folding 2 (0.57) (August 2006), one transcript was similar to a gene encod- Function not annotated 52 (14.86) ing a male fertility protein from both maize (Accession No hits found 90 (25.71) Number: NP_912416) and wheat (Accession Number: AAV70496) suggesting that this transcript has a role in These transcripts were pooled from clusters III, IV and V (Figure 5), with each individual transcript then allocated a functional category pollen maturation as opposed to meiosis. When examin- based on annotation and literature searches

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Category Representations (%) Histogram Expression Profile

Histone-related 15 (25.00)

Cell cycle regulation 14 (23.33)

Cytoskeletal- associated 10 (16.67)

Chromosome- associated 10 (16.67)

Recombination 7 (11.67)

Mismatch repair 2 (3.33)

Synaptonemal complex 1 (1.67)

Fertility-related 1 (1.67)

FunctionalFigure 6 classifications for the 60 meiosis and/or cell division transcripts identified from Table 1 Functional classifications for the 60 meiosis and/or cell division transcripts identified from Table 1. These transcripts were classified into functional categories based on the annotation obtained. The histogram represents the absolute values for each category, while the expression profiles for each of the candidates within each of the categories has also been shown. The red dotted line in the expression profile graphs represents the overall trend line for that category.

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Transcripts involved in early meiosis been described above) displayed analogous patterns The key aim of the experiments described here was to within our data set. Therefore it appears that the wheat identify genes that may be involved in controlling the genes identified here are indeed orthologues of the mei- early stages of meiosis. Therefore we were particularly otic genes identified in other organisms. Information on interested in transcripts that showed expression only in transcript abundance can help identify previously unchar- the early meiotic stages. These were identified based on acterized genes that may have roles in homologous transcripts with an RMA normalized value > 6 for either recombination. Such transcripts would show co-regula- PM or LP and < 5 for all stages thereafter. Interestingly tion with known meiotic genes from within this meiotic only four transcripts were identified, of which three data set. This assumption is supported by the close simi- (TaAffx.11970.3.S1_s_at, TaAffx.29005.1.S1_at and larities in expression profiles between two related mis- TaAffx.86700.1.S1_at) showed no significant similarity to match repair genes, TaMSH7 [39] and AtMLH1 [46] sequences in the NCBI and TIGR databases. The remain- (correlation coefficient of 0.997). ing transcript (Ta.400.2.A1_at) returned a significant hit of 6e-59 to a putative condensin complex subunit from rice In addition to the 'known' meiotic genes described above, (BLASTx). The condensin complex has been reported to the wheat data set contains many meiotic transcripts that have varying roles during both mitosis and meiosis, do not show significant similarity to sequences in the including chromosome segregation and spindle assem- NCBI and TIGR databases (E-value < e-10). Three of these bly. These genes are clearly prime candidates for further transcripts display radically different levels of expression study since they might have a role in coordinating the across the meiotic time course investigated (Figure 7). In early meiotic event of recombination. particular, the transcript corresponding to the Affymetrix probe set TaAffx.38162.1.S1_at displays an extreme From the 1,350 putative meiotic transcripts identified expression pattern in the microarray data. This expression through gene filtration, many appear to be orthologous to profile was confirmed in the Q-PCR analysis. With more genes from other organisms that are known to be involved than a four-fold drop from PM to LP, and then a rapid 64- in meiosis. Specifically, there are representatives of genes fold increase in expression between LP to T, this gene involved in processes such as synapsis, TaASY1 (an ortho- might encode a repressor of an event occurring within the logue of AtASY1, Arabidopsis asynapsis 1) (Boden et al., leptotene to pachytene stages such as chromosome pair- unpublished data). Furthermore, there are several mis- ing, synapsis or recombination. Significantly, there does match repair genes including wheat MutS homologue 2 not appear to be a transcript within the entire data set that (TaMSH2), wheat MutS homologue 6 (TaMSH6), and the previously characterised wheat MutS homologue 7 14 (TaMSH7) [39]. Other putative meiotic transcripts identified within the microarray data include candidates for recombination, such as radiation sensitive RAD51B and 12 RAD51C, disrupted meiotic cDNA (DMC1) and the rice replication protein A1 (RPA). Osakabe and colleagues 10 [40] and Bleuyard and colleagues [41] have previously characterised Arabidopsis RAD51B (AtRAD51B) and found 8 that it is important for double stranded DNA break repair in somatic cells. RAD51C on the other hand, is necessary for homologous recombination in meiosis and mitosis base 2) (log levels Expression 6 [41-43]. From previously published research, it is evident that RPA is essential for various aspects of DNA metabo- 4 lism in eukaryotes [for review see [44]]. In rice and Arabi- PM LP DA TT T IP MAN dopsis there are two different types of RPA [45] with inactivation of the AtRPA70a resulting in lethality, thus ThreeacrossFigure novelthe 7 seven candidates stages withinvestigated significant expression variability suggesting a role in DNA replication. However, even Three novel candidates with significant expression variability across the seven stages investigated. though the phenotype appeared normal under standard TaAffx.38162.1.S1_at (blue), TaAffx.9800.1.S1_at (black) and growth conditions, disruption of AtRPA70b resulted in TaAffx.60258.2.S1_s_at (red) are highlighted. hypersensitivity to mutagens such as UV-B and methyl TaAffx.38162.1.S1_at shows more than a 64-fold increase in methanesulfonate. This implied a role in DNA repair expression from LP to T, while TaAffx.9800.1.S1_at drops processes [45]. approximately 64-fold from PM to T. TaAffx.60258.2.S1_s_at is also down-regulated from PM to T approximately 16-fold. Many of the transcripts with significant similarities to pre- PM, LP, DA, TT, T, IP and MAN are as described in Figure 1. viously characterised meiotic genes (some of which have

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shares a similar expression profile to probe set addition to known meiotic genes will now form the basis TaAffx.38162.1.S1_at. Consequenly TaAffx.38162.1.S1_at for further research. The key objective of the study out- is a worthy candidate for further work to elucidate its role lined here, has been to provide a resource for meiosis during bread wheat meiosis. research that can link the strong cytogenetic, genetic and practical research base of wheat to the detailed biochemi- Q-PCR confirmation of microarray data cal and molecular information now emerging from model Q-PCR was conducted in order to validate representative organisms such as yeast. microarray results and examine the correlation between the two expression profiling platforms. A total of 15 Methods primer sets were designed to amplify fragments represent- Tissue isolation and RNA extraction ing probe sets on the Affymetrix GeneChip® (Table 2). Wild-type wheat (Triticum aestivum L. cv. Chinese Spring) Transcripts were selected based on their meiotic expres- was grown in a temperature-controlled glass house at sion profiles and similarity to known meiotic genes 23°C (day) and 15°C (night) with a 14 hour photope- (where there was an expression profile to support conser- riod. Anthers were collected and dissected using a Leica vation of function). MZ6 dissecting microscope. Anther squashes were prepared in order to determine the stage of meiosis. The microarray and Q-PCR profiles were closely related. Squashed anther preparations were viewed using a Leica Correlation coefficients ranged from R = 0.73 to R = 0.98, DM1000 compound microscope. with the exception of one outlier (R = 0.50) (Figure 8). The median correlation coefficient for the microarray/Q- The seven stages collected were pre-meiosis (PM), lepto- PCR data set was R = 0.95. Overall expression patterns tene to pachytene (LP), diplotene to anaphase I (DA), tel- were similar, confirming a high degree of reproducibility ophase I to telophase II (TT), tetrads (T), immature pollen between the two platforms. These results parallel those of (IP) and mature anthers (MAN). Immediately after deter- Honys and Twell [47] and Shary and colleagues [48] who mining the stage, the remaining two anthers from the flo- showed similar levels of correlation with reverse transcrip- ret were placed into liquid nitrogen. After collecting at tion PCR and northern blots, respectively. least 25 staged anthers for each time point from several biological samples, anthers from the respective stages A pairwise comparison between the Q-PCR results high- were pooled. Leaf material used in this study was collected lighted co-expression between many of the transcripts from glasshouse-grown plants (six weeks) and total RNA (Table 3) with a significant number of these transcripts isolated using Trizol® (Gibco BRL, Australia) according to having a correlation of over 0.9. These findings suggest the manufacturer's protocol. that there are a discrete number of transcription factors that control meiotic genes and hence the regulation of Microarray processing meiotic progression in bread wheat, as has been suggested aRNA from the seven stages were amplified and labelled for yeast [49,50]. In order to further our understanding of from one microgram of total RNA with two rounds of meiotic regulation and determine whether any of these amplification. The GeneChip® Two-Cycle cDNA Synthesis candidates are co-regulated, a yeast one-hybrid approach Kit (Affymetrix, CA, USA) was used to produce reverse could be employed using the promoter regions of the can- transcribed double-stranded cDNA containing a T7 pro- didates. moter, which was in vitro transcribed using the Ambion Megascript T7 amplification kit (Ambion, TX, USA). This Conclusion unlabelled aRNA was subsequently reverse transcribed to The transcript profiling information generated in this double stranded cDNA using the GeneChip® Two-Cycle study was designed to help decipher the bread wheat mei- cDNA Synthesis Kit and biotin labelled aRNA was then ome as an important step to manipulate pairing and produced using the GeneChip® IVT Labelling Kit (Affyme- recombination in plant breeding programs. Over 1,300 trix, CA, USA). Twenty micrograms of aRNA from each of transcripts showed meiotic regulation over the tissue the seven samples were fragmented for hybridization to series used in this study, with 467 novel transcripts iden- each microarray. In total three technical replicates were tified. Through hierarchical clustering 60 meiosis and/or conducted for each of the seven stages examined. Affyme- cell division candidates were identified as meiotically-reg- trix GeneChip® Wheat Genome Arrays were used for all ulated. Histone-related, chromosome-associated, recom- samples. The arrays were hybridized and processed bination and fertility candidates were among those according to the manufacturer's specifications. identified in this group. Through comparison with similar research in simpler eukaryotes, it has been possible to Microarray analysis draw parallels with the more complex genome of hexa- Normalization of the microarray data was conducted ploid bread wheat. A select number of novel candidates in using RMA. The software package Acuity 4 (Molecular

Page 11 of 17 (page number not for citation purposes) BMC Genomics 2006, 7:267 http://www.biomedcentral.com/1471-2164/7/267 Table 2: Primer sets used in Q-PCR analysis. PrimersetsusedinQ-PCR Table 2: A5BTa.7197.1.A1_at Ta.24096.1.S1_at RAD51B PHS1 MSH6 A5CTa.10540.1.S1_at RAD51C M Ta.25342.1.S1_at WM5 Ta.25861.1.A1_at Ta.30833.1.S1_at MSH4 DMC1 A5 Ta.7706.1.S1_at RPA RAD54 ASY1 M4Ta.30383.1.A1_at Ta.28776.1.A1_at WMC4 WMC3* Cyclophilin Controls TaAffx.38162.1.S1_at Ta.3385.1.A1_at WMC10* WMC6 * indicates those transcriptsthat have an unclear orientation(not known whetherantisense). sense or to theacquisition temperatures used.Controlgenesinitalicswere addition Primer setsusedandtheproductsizesobtainedin Sense temperature Acquisition Affymetrix probeset Candidate M5Ta.3224.2.S1_at WMC5 ltgn Ta.28350.1.S1_a_at Ta.9657.1.S1_at 2 gene Flat 1 gene Flat Actin GAPdH EFA1 Ta.6986.1.S1_at Ta.9186.1.S1_at TaAffx.47591.1.S1_at 83 80 82 78 80 81 79 81 79 82 83 81 80 83 80 83 80 77 82 79 80 GCTGTCGCAAACCCTTTCG GCTGAGGAAAGGCAAAGGCG TATTGATACAGAGGGCAGTTTC CTTGCTGCT CATCGAGTGGGCTTTAGCTATAG Sequence CCGTCTTTATGACGACAGTTCCTAC160 GAAGCGACGATGTCCACATGACC ACGCAGCTACCTGTATCATTCGGATC CCCTCAGACCGCTGGCAA TTCAACATCATTCCAAGCAGCA CAGATTGGCAACGGCTACG AGGACTCCCACAAGCAATCG CTGCCTGGCTGAAGCTGAAG CTGAAGGATGGTGTCCG GATTCCCAAATGTTCGAC GAATGTCTTCCGTGAACCG TGATGCTGCTGGTGGAAATTCG CAAGCCGCTGCACTACAAGG GATGCTAAGTAGAGGCCTAAGACACAT 166 GCCACTTCACATGCACCCATCTAATC AGGAGTTGACATGACAAGATTAGGGAGG CGGACAGTCCAGATGTGC CGACCGACGGAATTGATATG CATAATATTGGCACAGATTGGAG GACAATGGAACCGGAATGGTC CCCAATGATAATTC ACG those selectedbygeNormfor normalisation. ATACGCGTACTC245 CAGTTAGCTGCCAGGTCATCTTTC GTCGACTTTGTT195 CGGTGCAGTAGCCTTTGTCGATTT TGAGACACTCT 344 GTCGTAGGCACCAATCATCCATC AGGTCCTGCAATGCTTCACG Antisense Sequence AGCTGCATATTCGGAAGTAG ACCTGAGTGTCA 178 CAACACGTAGTACGATAGATCCAAG AGGGGACGGTGCAGATGAA ACAGAGGGTG274 CATCTAAGGACGGGTGCTAG TTAGCGTTCCA 236 GTGTGATGCCAGATTTTCTCCAT TTAAGTCGATT 171 CTGTGAGAAGTTTCAGCATTATC AGGAAAAGAGA300 GAGGCGGACAGACATGGAAGAA 227 CGGACAGCAAAACGACCAAG GAATGCTAAGG270 CGGACACTAGGCATGATAGGCG CGTAACCCAAAATGCCCTTG CTATGCTTGCTGCCTGATG CTCGAGTGCC159 ACCTGCTGGAGGATCGGCTC CTGACGAAAGCACGGAAGC CAAATTGTCCTCCTTACG AAACACACAGGG267 GATAGAACAAGCAAACTATGGGAG Product size(bp) 227 266 252 173 271 220 161

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ASY1 (0.98) DMC1 (0.98) MSH4 (0.88) 2 2 4 4 1.0 1.0

1 1 0.5 0.5 2 2

0 0 0.0 0.0

0 0 -1 -1 -0.5 -0.5

-2 -2 -1.0 -1.0 -2 -2

-3 -3 -1.5 -1.5

-4 -4 -4 -4 -2.0 -2.0

-5 -5 -6 -6 -2.5 -2.5 PM LP DA TT T IP MAN PM LP DA TT T IP MAN PM LP DA TT T IP MAN

MSH6 (0.73) PHS1 (0.95) RAD51B (0.96)

2 2 2 2 2 2

1 1 1 1

0 0 0 0 0 0

-1 -1 -1 -1 -2 -2 -2 -2

-2 -2 -3 -3

-3 -3 -4 -4 -4 -4

-5 -5 -4 -4 PM LP DA TT T IP MAN PM LP DA TT T IP MAN PM LP DA TT T IP MAN RAD51C (0.78) RAD54 (0.96) RPA1 (0.98) 1.0 1.0 3 2 2

2 2 0.5 0.5 0 0 1

0.0 0.0 0 0 -2 -2

-0.5 -0.5 -1

-4 -4 -2 -2 -1.0 -1.0

-3 -6 -6 -1.5 -1.5 -4 -4

-2.0 -2.0 -5 -8 -8 PM LP DA TT T IP MAN PM LP DA TT T IP MAN PM LP DA TT T IP MAN

WM5 (0.97) WMC3 (0.50) WMC4 (0.94) 2 2 2 2 2 2

1 1 1 1 1 1

0 0 0 0 0 0 -1 -1 -1 -1 -2 -2 -1 -1 -2 -2 -3 -3

-2 -2 -3 -3 -4 -4

-4 -4 -3 -3 -5 -5 PM LP DA TT T IP MAN PM LP DA TT T IP MAN PM LP DA TT T IP MAN

WMC5 (0.76) WMC6 (0.93) WMC10 (0.98) 2 2 2 2 6 6

4 4 1 1 1 1

2 2 0 0 0 0 0 0 -1 -1 -2 -2 -1 -1 -2 -2 -4 -4

-2 -2 -3 -3 -6 -6

-4 -4 -3 -3 -8 -8 PM LP DA TT T IP MAN PM LP DA TT T IP MAN PM LP DA TT T IP MAN

CorrelationFigure 8 of the microarray profile with the Q-PCR data from the corresponding transcript Correlation of the microarray profile with the Q-PCR data from the corresponding transcript. Lines with the open circles represent microarray data, while lines with solid circles represent the Q-PCR data. The data for each transcript from the microarray is log base 2, RMA normalized and centered about its average across the seven stages, while the data for the Q-PCR is log base 2, normalized mRNA copies/L and centered. Correlation values for each of the transcripts investigated using both technology platforms are indicated.

Page 13 of 17 (page number not for citation purposes) BMC Genomics 2006, 7:267 http://www.biomedcentral.com/1471-2164/7/267 Table 3:Q-PCR correlation of15 candidates with one another. italicized. Q-PCR products with a transcript correlation greater than or equal to 0.95 and less than 1 are in bold, while correlations smal TaWMC#4 TaWMC#3 TaWM5 TaRPA TaRAD54 TaPHS1 TaMSH6 TaDMC1 TaASY1 TaWMC#10 0.94 TaWMC#6 TaWMC#5 aA5C 0.93 TaRAD51CS 0.94 TaRAD51B 0.90 TaMSH4 aS1TDC aS4TMH aH1TRD1 TaRAD5 TaRAD51B TaPHS1 TaMSH6 TaMSH4 TaDMC1 TaASY1 .708 .708 .907 .408 .407 1.00 0.78 0.84 0.83 0.84 0.76 0.99 0.79 0.99 0.96 0.89 0.99 1.00 0.67 0.97 0.99 0.84 0.97 0.87 0.99 0.97 0.98 0.99 0.99 0.99 0.98 0.97 0.98 0.97 0.98 0.99 0.98 1.00 07 06 04 07 06 07 07 06 06 05 09 06 06 06 1 -0.62 -0.68 -0.65 -0.93 -0.59 -0.69 -0.68 -0.70 -0.71 -0.62 -0.74 -0.46 -0.65 -0.74 0.96 0.97 .809 .70.99 0.97 0.97 0.98 .707 .908 1.00 0.88 0.89 0.96 0.76 0.87 0.95 1.00 0.93 0.92 0.94 0.92 1.00 0.94 .90.99 0.99 0.97 0.98 0.96 0.95 1.00 .70.99 0.97 1.00 .20.94 0.91 1.00 0.92 0.79 0.89 0.87 0.89 0.80 .50.98 0.95 .609 .91.00 0.99 0.99 0.98 0.96 0.99 0.95 .509 .90.96 0.99 0.95 0.95 0.97 C aA5 aP aM aM# aM# aM# aM# TaWMC#10 TaWMC#6 TaWMC#5 TaWMC#4 TaWMC#3 TaWM5 TaRPA TaRAD54 1CS 1.00 0.94 .70.97 0.97 1.00 1.00 0.81 .21.00 0.82 0.82 ler than 0.95 but greater than or equal to 0.9 are .80.97 0.98 0.98 1.00 1.00

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Devices, CA, USA) was then used to analyze the microar- Reverse Transcriptase (Invitrogen, Australia) according to ray data. Microarray expression ratios were presented as the manufacturer's instruction. log-transformed base 2. Gene annotations were obtained through batch BLASTs (BLASTx; E-value < e-10) using the For each gene investigated using Q-PCR, a dilution series Affymetrix probe set sequences in tandem with sourcing covering seven orders of magnitude was prepared from annotations directly from the Affymetrix website. In total, 109 copies/L stock solution as detailed in Burton and col- 412 'rogue' probe sets were discarded from the analysis leagues [52]. Three replicates of each of the seven standard due to technical problems during the microarray process- concentrations were included with every Q-PCR experi- ing. ment together with a minimum of three no template controls. Q-PCR experiments were assembled by a liquid All p-values referred to in the text are corrected p-values handling robot, a CAS-1200 robot (Corbett Robotics, Aus- that were obtained using student's t-tests assuming equal tralia). Three replicate PCRs for each of the cDNAs were variances and using the Benjamini-Hochberg method included in every run. [51]. These p-values were used to determine whether transcripts were temporally-regulated during meiosis. Two L of the cDNA solution or the diluted standard or water was used in a reaction containing 5 L of IQ SYBR Suitable probe sets from the 1,350 transcripts used for Green PCR reagent (Bio-Rad Laboratories, California, expression analysis in the developing wheat anther were USA), 1.2 L each of the forward and reverse primers at 4 selected based on several criteria. Probe sets designated by M, 0.3 L of 10X SYBR Green in water and 0.3 L of Affymetrix not to cross-hybridize outside of their gene water. The total volume of this PCR was 10 L. family were selected if they had a consensus sequence > 250 bp and had a BLASTx match with an E-value < e-30. Reactions were performed in a RG 3000 Rotor-Gene Real The 633 transcripts that remained were then assigned to Time Thermal Cycler (Corbett Research, Australia) as fol- functional categories of interest based on literature lows; 3 minutes at 95°C followed by 45 cycles of 1 second searches of the BLASTx matches. The average of the pre- at 95°C, 1 second at 55°C, 30 seconds at 72°C and 15 sec- meiosis (PM) values for each respective functional cate- onds at the optimal acquisition temperature described in gory was then subtracted from every data point. The line Table 2. A melt curve was obtained from the product at the graphs and box and whisker plots presented here were end of the amplification by heating from 70°C to 99°C. produced using Sigma Plot (Version 9) (Systat Software, Using the Rotor-Gene V6 software (Corbett Research, Aus- IL, USA). tralia) the optimal cycle threshold (CT) was determined from the dilution series, with the raw expression data Hierarchical clustering analysis focussed on transcript derived. The mean expression level and standard devia- expression patterns rather than absolute values and the tion for each set of three replicates for each cDNA was cal- triplicate data over the seven stages was averaged. The culated. average of every row (that is, every transcript) was then subtracted from every signal intensity in the gene expres- Quantitative Real-Time PCR normalisation sion matrix. The rows were then clustered using a Eucli- The normalisation strategy by Burton and colleagues [52] dean squared similarity metric and the average linkage was used in this time course experiment. Four control method. Acuity 4.0 (Molecular Devices, CA, USA) was genes were assessed (actin, GAPdH, EFA and cyclophilin). also used to apply principal component analysis to the The three best control genes from this set were selected, data set. with normalisation factors calculated using the geNorm program [53]. Microarray data set The microarray data set has been deposited in the Gene While these genes have been used in other studies the con- Expression Omnibus (GEO) database (Accession: sistency of expression of the best three control genes in GSE6027). this case was found to be poor. A measure of consistency was obtained by examining the M value [53], where a high cDNA synthesis and Quantitative Real-Time PCR M value indicates that a control gene has a very disparate Seven independent cDNA synthesis reactions were made expression with respect to other control genes. The highest for the staged anthers (PM, LP, DA, TT, T, IP and MAN) M value from the best three genes in these experiments using the same RNA that was hybridized to the wheat was approximately 1.7. Based on other time course exper- GeneChip®. RNA (1 g) was used as template for the iments conducted, we anticipated M values of approxi- cDNA synthesis reaction with Superscript III RNAse H- mately 1.0. To address this concern, further control genes were tested until an acceptable M value was obtained. Two

Page 15 of 17 (page number not for citation purposes) BMC Genomics 2006, 7:267 http://www.biomedcentral.com/1471-2164/7/267

additional genes were selected from the microarray data 9. Reinke V, Smith HE, Nance J, Wang J, Van Doren C, Begley R, Jones SJM, Davis EB, Scherer S, Ward S, Kim SK: A global profile of (Ta.9657.1.S1_at and Ta.28350.1.S1_a_at) in addition to germline gene expression in C. elegans . Mol Cell 2000, the four 'standard' Q-PCR control genes mentioned 6:605-616. above. 10. Schlecht U, Demougin P, Koch R, Hermida L, Wiederkehr C, Descombes P, Pineau C, Jegou B, Primig M: Expression profiling of mammalian male meiosis and gametogenesis identifies Selection criteria imposed for identifying the additional novel candidate genes for roles in the regulation of fertility. control transcripts were based on a similar strategy to Mol Biol Cell 2004, 15:1031-1043. 11. Pang AL, Johnson W, Ravindranath N, Dym M, Rennert OM, Chan Czechowski and colleagues [54]. Additionally, the signal WY: Expression profiling of purified male germ cells: stage- intensities were greater than five (log base 2) in all 21 specific expression patterns related to meiosis and postmei- otic development. Physiol Genomics 2006, 24:75-85. arrays with the triplicate data for the transcripts having a 12. Bennett MD: The duration of meiosis. Proc R Soc London Ser B standard deviation of less than 0.1. Probes sets that 1971, 178:277-299. Affymetrix denoted as being likely to cross hybridize were 13. Bennett MD, Chapman V, Riley R: The duration of meiosis in pollen mother cells of wheat, rye and Triticale . Proc R Soc London not selected. After re-calculating the normalization factors Ser B 1971, 178:259-275. using geNorm, the highest M value from the three best 14. Bennett MD, Smith JB: The effects of polyploidy on meiotic duration and pollen development in cereal anthers. Proc R Soc control genes was reduced to 0.68 and the raw expression London Ser B 1972, 181:81-107. values for the genes of interest in each cDNA were divided 15. Bennett MD, Finch RA, Smith JB, Rao MK: The time and duration by the normalization factor for that cDNA to produce the of female meiosis in wheat, rye and barley. Proc R Soc London Ser B 1973, 183:301-319. normalized expression data. 16. Roberts MA, Reader SM, Dalgliesh C, Miller TE, Foote TN, Fish LJ, Snape JW, Moore G: Induction and characterization of Ph1 wheat mutants. Genetics 1999, 153:1909-1918. Authors' contributions 17. Martinez-Perez E, Shaw P, Moore G: The Ph1 locus is needed to WC conducted the research, analyzed the data and drafted ensure specific somatic and meiotic centromere association. the manuscript. UB and TS designed the research, ana- Nature 2001, 411:204-207. 18. Prieto P, Shaw P, Moore G: Homologue recognition during mei- lyzed the data and drafted the manuscript. NS, TW and GS osis is associated with a change in chromatin conformation. contributed analytical tools and analyzed the data. PL Nat Cell Biol 2004, 6:906-908. designed the research and drafted the manuscript. JAA 19. Tanksley SD, Zamir D, Rick CM: Evidence for extensive overlap of sporophytic and gametophytic gene expression in tomato. designed and conducted the research, analyzed the data Science 1981, 213:453-455. and drafted the manuscript. All authors read and 20. Gorla MS, Frova C, Binelli G, Ottaviano E: The extent of gameto- approved the final manuscript. phytic-sporophytic gene expression in maize. Theor Appl Genet 1986, 72:42-47. 21. 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Quantitative analysis of transcripts available free of charge to the entire biomedical community reveals two groups of co-expressed genes. Plant Physiol 2004, peer reviewed and published immediately upon acceptance 134:224-236. 53. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De cited in PubMed and archived on PubMed Central Paepea A, Speleman F: Accurate normalization of real-time yours — you keep the copyright quantitative RT-PCR data by geometric averaging of multi- Submit your manuscript here: BioMedcentral http://www.biomedcentral.com/info/publishing_adv.asp

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^^^^^^^^^@^ ^0 " !# ^^ ! ^! "^ " ^ ^ ! !^ "^^ "" ^q^ E p ! g^ " g^ ^ ^" g^" ^b^ ^ ^^^# ^# f^ ! !^ ^ ^ ^%"# ^ ""a^^ ^ "^^ ^ ^ !^^ ! !^ ^ ^ ^%"# ^ ""F^ @^ ^^ ^ ! !^ # ^! ^## # ^ ^ "!^ ^ ^ "#" ^ ^ "^ " ^ ^^" ^ # g^^ ""^ !^ ^ i"^ ^^ aG

^^ G^ G^ G^ ^ xG^ ^ BOMGS^ QQGYKZMOUSGJOROQOGIGJUML^ GQQYKZMOUSGJUJTTQ^ ^ ^ ^ ^

^ jlh