Prediction of components of the sporopollenin synthesis pathway in peach by genomic and expression analyses
© Ríos et al.; licensee BioMed Central Ltd. 2013
Received: 16 October 2012
Accepted: 15 January 2013
Published: 18 January 2013
The outer cell wall of the pollen grain (exine) is an extremely resistant structure containing sporopollenin, a mixed polymer made up of fatty acids and phenolic compounds. The synthesis of sporopollenin in the tapetal cells and its proper deposition on the pollen surface are essential for the development of viable pollen. The beginning of microsporogenesis and pollen maturation in perennial plants from temperate climates, such as peach, is conditioned by the duration of flower bud dormancy. In order to identify putative genes involved in these processes, we analyzed the results of previous genomic experiments studying the dormancy-dependent gene expression in different peach cultivars.
The expression of 50 genes induced in flower buds after the endodormancy period (flower-bud late genes) was compared in ten cultivars of peach with different dormancy behaviour. We found two co-expression clusters enriched in putative orthologs of sporopollenin synthesis and deposition factors in Arabidopsis. Flower-bud late genes were transiently expressed in anthers coincidently with microsporogenesis and pollen maturation processes. We postulated the participation of some flower-bud late genes in the sporopollenin synthesis pathway and the transcriptional regulation of late anther development in peach.
Peach and the model plant Arabidopsis thaliana show multiple elements in common within the essential sporopollenin synthesis pathway and gene expression regulatory mechanisms affecting anther development. The transcriptomic analysis of dormancy-released flower buds proved to be an efficient procedure for the identification of anther and pollen development genes in perennial plants showing seasonal dormancy.
Sexual reproduction in angiosperms involves the formation of complex reproductive organs (flowers) containing diploid tissues and the haploid germline. The germline gives rise to the male (pollen) and female gametophyte (embryo sac) through successive meiotic and mitotic cell divisions from their respective microspore and megaspore mother cells. The genetic and molecular regulation of these events has been extensively studied in the model species Arabidopsis thaliana[1–3]. Pollen development and maturation occurs within the anther locule, surrounded by a specialized layer of helper cells named the tapetum. Tapetal cells greatly contribute to pollen viability and function through the segregation and deposition of the outer cell wall layer (exine) and the pollen coat (tryphine) on the pollen surface. The exine is an extremely durable and biochemically resistant structure consisting of sporopollenin, a series of complex polymers derived from fatty acids and phenolic compounds; whereas tryphine contains a sticky mixture of fatty acids, flavonoids, carotenoids and proteins deposited on the exine surface and cavities when the tapetum degenerates through programmed cell death [4, 5].
Recently, several biochemical steps of sporopollenin biosynthesis and transcriptional regulatory circuits controlling pollen development have been elucidated in Arabidopsis by the analysis of male-sterile and exine-defective mutants . In brief, medium- to long-chain fatty acids such as lauric acid are monohydroxylated by the cytochrome P450 CYP703A2 , and modified to form fatty acyl-CoA esters by ACYL-COA SYNTHETASE5 (ACOS5) in tapetal cells . CoA-esterified fatty acids are alternatively reduced to form fatty alcohol derivatives or condensed with malonyl-CoA by LESS ADHESIVE POLLEN5/POLYKETIDE SYNTHASE B (LAP5/PKSB) and LAP6/PKSA, leading to alkyl pyrones [9, 10]. These latter compounds are hydroxylated by TETRAKETIDE α-PYRONE REDUCTASE1 (TKPR1) and TKPR2 , and combined with phenylpropanoids to produce the sporopollenin precursors. Then sporopollenin is successively secreted to the apoplast by specific transporters  and translocated to the microspores bound to proteins such as lipid transfer proteins (LTPs) and glycine rich proteins (GRPs) . A network of transcription factors containing basic helix-loop-helix (bHLH), plant homeodomain (PHD) finger, and MYB domains among others are likely regulating the expression of genes involved in these processes in the tapetum [13–18].
The knowledge regarding tapetum and pollen development in species other than the model organisms such as Arabidopsis and rice is scarce and fragmentary; in spite of the relevant influence that these processes exert on pollen viability, fruit set and productivity. Within the genus Prunus, including stone-fruit species as peach, plum, apricot, almond and cherry, several agronomical reports describe male-sterile varieties at the morphological and histological level [19–22]. However a consistent genetic and genomic analysis of processes affecting pollen viability is currently non-existent. The pollen development in Prunus species and other woody perennial plants from temperate climates such as apple and poplar is affected by the seasonal cessation of meristem growth termed endodormancy. Endodormancy contributes to elude the detrimental effects of the low temperatures in winter by preventing the resumption of growth under non-optimal conditions for survival. The growth inhibition of endodormant buds is due to internal signals within the buds, in contrast to growth inhibition by other distal organs (paradormancy), or by environmental factors (ecodormancy). For the purpose of this work we have employed the term dormancy to refer to the endodormant state. In these species, the flower buds start to differentiate in summer and continue their reproductive development until growth is arrested in autumn. After a period of chilling accumulation required for dormancy release, pollen mother cells within the anthers initiate meiosis and further microspore development, resulting in fully mature pollen grains .
In order to identify putative genes involved in tapetum function, pollen development and pollen wall formation in peach (Prunus persica [L.] Batsch), we analyzed the results of two transcriptomic experiments comparing gene expression between dormant and dormancy-released flower buds, and in peach cultivars with different dormancy behaviour [24, 25]. This work led us to postulate a role for several genes in sporopollenin synthesis and deposition, and transcriptional regulation of pollen development processes, based on expression analysis and previous works in model species.
Results and discussion
Identification of genes up-regulated in late stages of reproductive bud development (flower-bud late genes)
Flower-bud late genes obtained in transcriptomic studies in peach
Number of ESTs
Putative ortholog in Arabidopsis*
Protease inhibitor/seed storage/LTP
Protease inhibitor/seed storage/LTP
Protease inhibitor/seed storage/LTP
BURP domain protein
BURP domain protein
BURP domain protein
DNA-binding protein (AT-hook)
Protease inhibitor/seed storage/LTP
Chlorophyll A-B binding protein
Protease inhibitor/seed storage/LTP
PHD Zn-finger protein
BURP domain protein
MazG nucleotide pyrophosphohydrolase
Early nodulin 93 ENOD93 protein
Protein of unknown function (DUF538)
Microsomal signal peptidase subunit
Helix-loop-helix DNA-binding domain
XYPPX repeat protein
Protein of unknown function (DUF668)
ATPase family (AAA)
Flower-bud late genes are expected to play a role in dormancy release, growth resumption or late flowering events. Whereas DORMANCY ASSOCIATED MADS-box (DAM) and other genes found repressed in dormancy-released buds have been unequivocally related to dormancy processes [32, 33], no experimental evidences have been obtained pointing to a role of flower-bud late genes described in this work in dormancy processes. In order to identify putative orthologs of these genes in Arabidopsis we made a reciprocal blast analysis (RBA) as described in Methods. Interestingly, 13 genes were putative orthologs of Arabidopsis genes involved in sporopollenin synthesis and transcriptional regulation of tapetum and pollen development (Table 1, Additional file 1). In addition, ppa009789m was very similar to RUPTURED POLLEN GRAIN1 (RPG1), a component of the MtN3/saliva gene family coding for a plasma membrane protein essential for microspore viability and exine pattern formation in Arabidopsis, even though they could not be considered as putative orthologs by RBA (Table 1). These data strongly suggest that flower-bud late genes identified by two transcriptomic approaches in peach [24, 25] are to a large extent involved in sporopollenin synthesis and deposition, indicating the activation of this metabolic pathway during or shortly after dormancy release. Such predominance of pollen cell wall related genes over other bud processes, as dormancy release, abiotic stress resistance and female gametophyte development, could be due to the major contribution of anthers to the total weight of the bud, or alternatively could be caused by an experimental bias of the SSH procedure towards transcripts with higher expression differences.
Flower-bud late genes show cultivar-dependent expression
Flower-bud late genes are transiently expressed in anthers
Based on qRT-PCR results shown in Figures 4 and 5, we have determined that flower-bud late genes are transiently expressed in anthers with slight differences in the timing of induction. These results reasonably suggest that cluster-specific differences observed in Figures 2 and 3 are due to differences in the induction time instead of the presence of distinct signals and transduction pathways. Under this hypothesis, cultivar-specific features of clusters A and B and non-clustered genes (Figure 3) could merely describe snapshots of a single transcriptional program taken at different times. Most of cluster B genes are expressed later, leading to cultivar-specific differences at the fixed collection point of 400 chilling hours observed in Figure 3B. On the contrary, earlier non-clustered genes could have acquired a similar maximum expression level at this fixed time in different cultivars (Figure 3C), and A genes could represent an intermediate situation between B and non-clustered genes (Figure 3A). A highly simplified interpretation of these data would suggest the induction of A genes by one or several non-clustered regulatory genes, and the successive expression of B genes induced by a hypothetical transcriptional factor activated or expressed concomitantly with A genes. However a better knowledge on the transcriptional networks affecting tapetum and pollen processes is required to ascertain the plausibility of this hypothesis.
Flower-bud late genes are expressed during microsporogenesis and pollen maturation processes
Flower-bud late genes were not significantly expressed in samples 1 (dormant buds) and 5 (mature pollen grains), thus they are expected to be involved in one or several processes occurring in samples 2 to 4, as meiotic and mitotic cell division, pollen maturation, synthesis and segregation of substances, and tapetum degeneration. Tapetal cells actively participate in the supply of essential compounds for pollen cells during most of the period covered by these samples and particularly are involved in the synthesis and deposition of sporopollenin; a major component of the pollen cell wall exine. The exine may be identified as a blue light layer surrounding the vacuolated microspores and pollen grains stained in Figures 6D-E, but sporopollenin starts to accumulate earlier, in the tetrad stage  (Figure 6C). The temporal expression pattern of flower-bud late genes, peaking in samples 3 and 4 in anthers, in addition to their protein sequence similarity to sporopollenin-related genes of Arabidopsis, strongly suggest a role of some of these genes in sporopollenin synthesis and deposition, as detailed below.
Candidate genes for sporopollenin synthesis and deposition in peach
The following flower-bud late genes coding for putative DNA-binding and regulatory proteins could be involved in the transcriptional regulation of pollen maturation pathways: ppa008351m, ppa022178m and PpB71 (Figure 7). The Arabidopsis potential ortholog of ppa008351m (AtbHLH91/At2g31210) codes for a bHLH-type transcription factor that interacts at the protein level with ABORTED MICROSPORES (AMS) and DYSFUNCTIONAL TAPETUM 1 (DYT1), two other bHLH-type factors involved in tapetum development and pollen wall formation [17, 34].
On the other side, ppa022178m is the potential peach counterpart of the Arabidopsis MALE STERILITY1 (MS1) gene, which encodes a well-known PHD-domain transcription factor relevant for late tapetum development and pollen wall biosynthesis [15, 16, 18]. Interestingly, At2g42940 gene, coding for an AT-hook DNA-binding protein highly similar to peach PpB71, was found specifically expressed in the wild-type tapetum after meiosis, and unexpectedly up-regulated in the ms1 mutant . This prompted to the authors to hypothesize that MS1 was involved in the stage-specific repression of At2g42940 to ensure its expression in a narrow time interval soon after the degeneration of the callose walls surrounding the tetrads. The functional relevance of At2g42940 in pollen cell wall formation was assessed by the generation of RNAi transgenic lines, showing pollen grains with a thinner cell wall, some of which had collapsed .
The fact that genes expected to function downstream in the biochemical pathway (TKPRs, LTPs, GRPs) are expressed earlier than the upstream genes seems to be rather inconsistent (Figure 7). However their particular expression profiles do overlap over a certain period of time, suggesting that it could act as a mechanism ensuring the activation of this pathway at the precise time. The complex network of transcriptional and protein interactions between the transcriptional factors involved in early and late anther development in Arabidopsis[17, 18, 34, 35] points to an intricate gene regulation pathway. As inferred from the expression studies shown in this work, ppa008351m (bHLH) is expressed earlier than ppa022178m (PHD) and PpB71 (AT-hook) within the regulatory circuits operating in the anther developmental events in peach (Figure 7).
The data presented here constitute an initial genomic approach to unravel anther developmental processes in peach, focusing on sporopollenin synthesis and deposition. In addition, the identification of genes induced during microsporogenesis and pollen maturation processes could assist in the finding of expression biomarkers associated to dormancy release in peach .
This study utilized transcriptomic data from flower buds of peach at different stages of dormancy and several cultivars with different chilling requirements to obtain a list of flower-bud late genes expressed shortly after dormancy release. Some of these genes clustered into two major expression patterns. Their close similarity to genes described in the sporopollenin synthesis pathway in Arabidopsis and their transitory expression in anthers coinciding with microsporogenesis events strongly suggests their participation in the biochemical processes required for the formation of the cell wall exine of pollen grains. In addition, three peach regulatory factors with bHLH, PHD and AT-hook domains have been postulated to take part in transcriptional circuits regulating late anther development in peach.
The Prunus persica [L.] Batsch cv ‘86-6’, ‘Big Top’, ‘Carolina’, ‘Crimson Baby’, ‘Flor Red’, ‘May Glo’, ‘Precocinho’, ‘Red Candem’, ‘Rose Diamond’ and ‘Sunraycer’ were grown in an orchard located at the Instituto Valenciano de Investigaciones Agrarias (IVIA) in Moncada (Spain) under standard agricultural practices. The samples required for qRT-PCR of different cultivars were obtained from flower buds collected after a chilling accumulation of 400 chilling hours (hours below 7°C) . Flower buds of ‘Big Top’ cultivar for microscopy studies and time-dependent expression analysis were collected on the following dates of winter in 2012: 17 January (sample 1, after 460 chilling hours), 30 January (sample 2, after 603 chilling hours), 13 February (sample 3, after 775 chilling hours), 27 February (sample 4, after 936 chilling hours), and 12 March (sample 5, after 1038 chilling hours). Buds for the experiments described in Figure 4 were obtained from sample 3 (see above). Buds were routinely pooled from shoots obtained from three different adult trees.
Analysis of microarray data
Microarray data utilized in this study are stored in the ArrayExpress database (http://www.ebi.ac.uk/arrayexpress/) with accession number E-MEXP-3201. We generated a subset of microarray hybridization signals containing only genes and ESTs with higher expression in dormancy-released flower buds (flower-bud late genes) according to previous works [24, 25]. The hybridization signal intensity from those ESTs proceeding from the same gene was averaged to have a single hybridization value per gene for each of the ten cultivars used in the experiment. Clustering of gene expression data was performed in the platform Babelomics (http://babelomics.bioinfo.cipf.es/)  using the UPGMA method and the Pearson correlation coefficient as distance.
In order to identify putative orthologs of peach flower-bud late genes in Arabidopsis we performed a reciprocal blast analysis. First we made a blastp similarity search on Arabidopsis database using the predicted translated protein of flower-bud late genes as query. The first hit in the Arabidopsis genome was subsequently compared with the peach genome by tblastn search, and those genes found reciprocally by the searches in both the Arabidopsis and peach genomes were considered to be putative orthologs (Additional file 1).
Total RNA was isolated from 100 mg of tissue using the RNeasy Plant Mini Kit (Qiagen, Valencia, CA, USA), but adding 1% (w:v) polyvinylpyrrolidone (PVP-40) to the extraction buffer before use. From 1 to 2 μg of total RNA was reverse transcribed with PrimeScript RT reagent kit (Takara Bio, Otsu, Japan) in a total volume of 20 μl. Two microliter of a 20X diluted first-strand cDNA were used for PCR reactions in a final volume of 20 μl. Quantitative real-time PCR was performed on a StepOnePlus Real-Time PCR System (Life Technologies, Carlsbad, CA, USA), using SYBR premix Ex Taq (Tli RNaseH plus) (Takara Bio). Primer pairs are listed in Additional file 2. Cycling protocol consisted of 10 min at 95°C, followed by 40 cycles of 15 s at 95°C for denaturation, and 1 min at 60°C for annealing and extension. Specificity of the PCR reaction was assessed by the presence of a single peak in the dissociation curve after the amplification and through size estimation of the amplified product by agarose electrophoresis. We used as reference a peach actin transcript (ppa007211m) amplified with specific primers. Relative expression was measured by the relative standard curve procedure. Results were the average of two independent biological replicates with 2–3 technical replicates each.
Flower buds from ‘Big Top’ cultivar collected at five different dates (samples 1–5, see plant material) were fixed and embedded in London Resin White (London Resin, Woking, Surrey, UK) according to . Sections (about 1 micrometer thick) were cut with a Leica RM2255 microtome (Leica Microsystems, Wetzlar, Germany) using glass knives and fixed to microscope slides. Longitudinal-sections of buds were stained with 0.05% Toluidine Blue O (Merck, Darmstadt, Germany) and examined and photographed with a Leica DM LA microscope (Leica Microsystems).
We thank José Martínez, Enzo Stasi and José Palanca for technical assistance in the plant material maintenance. This work was supported by the Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA)-FEDER (grant no. RTA2007-00060), and the Ministry of Science and Innovation of Spain (grant no. AGL2010-20595). Carmen Leida was funded by a fellowship from IVIA.
- Ge X, Chang F, Ma H: Signaling and transcriptional control of reproductive development in Arabidopsis. Curr Biol. 2010, 20: R988-R997. 10.1016/j.cub.2010.09.040.View ArticlePubMed
- Berger F, Twell D: Germline specification and function in plants. Annu Rev Plant Biol. 2011, 62: 461-484. 10.1146/annurev-arplant-042110-103824.View ArticlePubMed
- Chang F, Wang Y, Wang S, Ma H: Molecular control of microsporogenesis in Arabidopsis. Curr Opin Plant Biol. 2011, 14: 66-73. 10.1016/j.pbi.2010.11.001.View ArticlePubMed
- Piffanelli P, Ross JHE, Murphy DJ: Biogenesis and function of the lipidic structures of pollen grains. Sex Plant Reprod. 1998, 11: 65-80. 10.1007/s004970050122.View Article
- Blackmore S, Wortley AH, Skvarla JJ, Rowley JR: Pollen wall development in flowering plants. New Phytol. 2007, 174: 483-498. 10.1111/j.1469-8137.2007.02060.x.View ArticlePubMed
- Ariizumi T, Toriyama K: Genetic regulation of sporopollenin synthesis and pollen exine development. Annu Rev Plant Biol. 2011, 62: 437-460. 10.1146/annurev-arplant-042809-112312.View ArticlePubMed
- Morant M, Jorgensen K, Schaller H, Pinot F, Moller BL, Werck-Reichhart D, Bak S: CYP703 is an ancient cytochrome P450 in land plants catalyzing in-chain hydroxylation of lauric acid to provide building blocks for sporopollenin synthesis in pollen. Plant Cell. 2007, 19: 1473-1487. 10.1105/tpc.106.045948.View ArticlePubMed
- de Azevedo SC, Kim SS, Koch S, Kienow L, Schneider K, McKim SM, Haughn GW, Kombrink E, Douglas CJ: A novel fatty Acyl-CoA Synthetase is required for pollen development and sporopollenin biosynthesis in Arabidopsis. Plant Cell. 2009, 21: 507-525. 10.1105/tpc.108.062513.View Article
- Kim SS, Grienenberger E, Lallemand B, Colpitts CC, Kim SY, de Azevedo Souza C, Geoffroy P, Heintz D, Krahn D, Kaiser M, Kombrink E, Heitz T, Suh DY, Legrand M, Douglas CJ: LAP6/POLYKETIDE SYNTHASE A and LAP5/POLYKETIDE SYNTHASE B encode hydroxyalkyl α-pyrone synthases required for pollen development and sporopollenin biosynthesis in Arabidopsis thaliana. Plant Cell. 2010, 22: 4045-4066. 10.1105/tpc.110.080028.View ArticlePubMed
- Dobritsa AA, Lei Z, Nishikawa S, Urbanczyk-Wochniak E, Huhman DV, Preuss D, Sumner LW: LAP5 and LAP6 encode anther-specific proteins with similarity to chalcone synthase essential for pollen exine development in Arabidopsis. Plant Physiol. 2010, 153: 937-955. 10.1104/pp.110.157446.View ArticlePubMed
- Grienenberger E, Kim SS, Lallemand B, Geoffroy P, Heintz D, de Azevedo Souza C, Heitz T, Douglas CJ, Legrand M: Analysis of TETRAKETIDE α-PYRONE REDUCTASE function in Arabidopsis thaliana reveals a previously unknown, but conserved, biochemical pathway in sporopollenin monomer biosynthesis. Plant Cell. 2010, 22: 4067-4083. 10.1105/tpc.110.080036.View ArticlePubMed
- Quilichini TD, Friedmann MC, Samuels AL, Douglas CJ: ATP-binding cassette transporter G26 is required for male fertility and pollen exine formation in Arabidopsis. Plant Physiol. 2010, 154: 678-690. 10.1104/pp.110.161968.View ArticlePubMed
- Zhang W, Sun Y, Timofejeva L, Chen C, Grossniklaus U, Ma H: Regulation of Arabidopsis tapetum development and function by DYSFUNCTIONAL TAPETUM1 (DYT1) encoding a putative bHLH transcription factor. Development. 2006, 133: 3085-3095. 10.1242/dev.02463.View ArticlePubMed
- Zhang ZB, Zhu J, Gao JF, Wang C, Li H, Li H, Zhang HQ, Zhang S, Wang DM, Wang QX, Huang H, Xia HJ, Yang ZN: Transcription factor AtMYB103 is required for anther development by regulating tapetum development, callose dissolution and exine formation in Arabidopsis. Plant J. 2007, 52: 528-538. 10.1111/j.1365-313X.2007.03254.x.View ArticlePubMed
- Yang C, Vizcay-Barrena G, Conner K, Wilson ZA: MALE STERILITY1 is required for tapetal development and pollen wall biosynthesis. Plant Cell. 2007, 19: 3530-3548. 10.1105/tpc.107.054981.View ArticlePubMed
- Ito T, Nagata N, Yoshiba Y, Ohme-Takagi M, Ma H, Shinozaki K: Arabidopsis MALE STERILITY1 encodes a PHD-type transcription factor and regulates pollen and tapetum development. Plant Cell. 2007, 19: 3549-3562. 10.1105/tpc.107.054536.View ArticlePubMed
- Xu J, Yang C, Yuan Z, Zhang D, Gondwe MY, Ding Z, Liang W, Zhang D, Wilson ZA: The ABORTED MICROSPORES regulatory network is required for postmeiotic male reproductive development in Arabidopsis thaliana. Plant Cell. 2010, 22: 91-107. 10.1105/tpc.109.071803.View ArticlePubMed
- Zhu J, Lou Y, Xu X, Yang ZN: A genetic pathway for tapetum development and function in Arabidopsis. J Integr Plant Biol. 2011, 53: 892-900. 10.1111/j.1744-7909.2011.01078.x.View ArticlePubMed
- Schwalm S, Hartmann W, Stosser R: Pollen development in male fertile and sterile plum cultivars (Prunus-domestica L ssp domestica). Gartenbauwissenschaft. 1995, 60: 145-150.
- Werner DJ, Creller MA: Genetic studies in peach: Inheritance of sweet kernel and male sterility. J Amer Soc Hortic Sci. 1997, 122: 215-217.
- Lillecrapp AM, Wallwork MA, Sedgley M: Female and male sterility cause low fruit set in a clone of the ‘Trevatt’ variety of apricot (Prunus armeniaca). Sci Hortic. 1999, 82: 255-263. 10.1016/S0304-4238(99)00061-8.View Article
- Radice S, Ontivero M, Giordani E, Bellini E: Anatomical differences on development of fertile and sterile pollen grains of Prunus salicina Lindl. Plant Syst Evol. 2008, 273: 63-69. 10.1007/s00606-008-0011-5.View Article
- Julian C, Rodrigo J, Herrero M: Stamen development and winter dormancy in apricot (Prunus armeniaca). Ann Bot. 2011, 108: 617-625. 10.1093/aob/mcr056.View ArticlePubMed
- Leida C, Terol J, Martí G, Agustí M, Llácer G, Badenes ML, Ríos G: Identification of genes associated with bud dormancy release in Prunus persica by suppression subtractive hybridization. Tree Physiol. 2010, 30: 655-666. 10.1093/treephys/tpq008.View ArticlePubMed
- Leida C, Conesa A, Llácer G, Badenes ML, Ríos G: Histone modifications and expression of DAM6 gene in peach are modulated during bud dormancy release in a cultivar-dependent manner. New Phytol. 2012, 193: 67-80. 10.1111/j.1469-8137.2011.03863.x.View ArticlePubMed
- Xing S, Zachgo S: ROXY1 and ROXY2, two Arabidopsis glutaredoxin genes, are required for anther development. Plant J. 2008, 53: 790-801. 10.1111/j.1365-313X.2007.03375.x.View ArticlePubMed
- Dobritsa AA, Nishikawa S, Preuss D, Urbanczyk-Wochniak E, Sumner LW, Hammond A, Carlson AL, Swanson RJ: LAP3, a novel plant protein required for pollen development, is essential for proper exine formation. Sex Plant Reprod. 2009, 22: 167-177. 10.1007/s00497-009-0101-8.View ArticlePubMed
- Alves-Ferreira M, Wellmer F, Banhara A, Kumar V, Riechmann JL, Meyerowitz EM: Global expression profiling applied to the analysis of Arabidopsis stamen development. Plant Physiol. 2007, 145: 747-762. 10.1104/pp.107.104422.View ArticlePubMed
- Lebel-Hardenack S, Ye D, Koutnikova H, Saedler H, Grant SR: Conserved expression of a TASSELSEED2 homolog in the tapetum of the dioecious Silene latifolia and Arabidopsis thaliana. Plant J. 1997, 12: 515-526. 10.1046/j.1365-313X.1997.d01-4.x.View ArticlePubMed
- Guan YF, Huang XY, Zhu J, Gao JF, Zhang HX, Yang ZN: RUPTURED POLLEN GRAIN1, a member of the MtN3/saliva gene family, is crucial for exine pattern formation and cell integrity of microspores in Arabidopsis. Plant Physiol. 2008, 147: 852-863. 10.1104/pp.108.118026.View ArticlePubMed
- Wilson ZA, Morroll SM, Dawson J, Swarup R, Tighe PJ: The Arabidopsis MALE STERILITY1 (MS1) gene is a transcriptional regulator of male gametogenesis, with homology to the PHD-finger family of transcription factors. Plant J. 2001, 28: 27-39. 10.1046/j.1365-313X.2001.01125.x.View ArticlePubMed
- Bielenberg DG, Wang Y, Li Z, Zhebentyayeva T, Fan S, Reighard GL, Scorza R, Abbott AG: Sequencing and annotation of the evergrowing locus in peach [Prunus persica (L.) Batsch] reveals a cluster of six MADS-box transcription factors as candidate genes for regulation of terminal bud formation. Tree Genet Genomics. 2008, 4: 495-507. 10.1007/s11295-007-0126-9.View Article
- Leida C, Conejero A, Arbona V, Gómez-Cadenas A, Llácer G, Badenes ML, Ríos G: Chilling-dependent release of seed and bud dormancy in peach associates to common changes in gene expression. PLoS One. 2012, 7: e35777-10.1371/journal.pone.0035777.View ArticlePubMed
- Feng B, Lu D, Ma X, Peng Y, Sun Y, Ning G, Ma H: Regulation of the Arabidopsis anther transcriptome by DYT1 for pollen development. Plant J. 2012, 72: 612-624. 10.1111/j.1365-313X.2012.05104.x.View ArticlePubMed
- Ma X, Feng B, Ma H: AMS-dependent and independent regulation of anther transcriptome and comparison with those affected by other Arabidopsis anther genes. BMC Plant Biol. 2012, 12: 23-10.1186/1471-2229-12-23.View ArticlePubMed
- Leida C, Romeu JF, García-Brunton J, Ríos G, Badenes ML: Gene expression analysis of chilling requirements for flower bud break in peach. Plant Breeding. 2012, 131: 329-334. 10.1111/j.1439-0523.2011.01946.x.View Article
- Medina I, Carbonell J, Pulido L, Madeira S, Goetz S, Conesa A, Tárraga J, Pascual-Montano A, Nogales-Cadenas R, Santoyo J, García F, Marbà M, Montaner D, Dopazo J: Babelomics: an integrative platform for the analysis of transcriptomics, proteomics and genomic data with advanced functional profiling. Nucl Acids Res. 2010, 38: W210-W213. 10.1093/nar/gkq388.View ArticlePubMed
- Tadeo FR, Tudela D, Primo-Millo E: 1-Aminocyclopropane-1-carboxylic acid-induced ethylene stimulates callus formation by cell enlargement in the cambial region of internodal explants of Citrus. Plant Sci. 1995, 110: 113-119. 10.1016/0168-9452(95)04173-R.View Article
This article is published under license to 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.