Primexine Formation Research Articles

ADAPTOR PROTEIN-1 complex-mediated post-Golgi trafficking is critical for pollen wall development in Arabidopsis.

Summary Primexine deposition is essential for the formation of pollen wall patterns and is precisely regulated by the tapetum and microspores. While tapetum‐ and/or microspore‐localized proteins are required for primexine biosynthesis, how their trafficking is established and controlled is poorly understood.In Arabidopsis thaliana, AP1σ1 and AP1σ2, two genes encoding the σ subunit of the trans‐Golgi network/early endosome (TGN/EE)‐localized ADAPTOR PROTEIN‐1 complex (AP‐1), are partially redundant for plant viability, and the loss of AP1σ1 function reduces male fertility due to defective primexine formation. Here, we investigated the role of AP‐1 in pollen wall formation.The deposition of Acyl‐CoA SYNTHETASE5 (ACOS5) and type III LIPID TRANSFER PROTEINs (LTPs) secreted from the anther tapetum, which are involved in exine formation, were impaired in ap1σ1 mutants. In addition, the microspore plasma membrane (PM) protein RUPTURED POLLEN GRAIN1 (RPG1), which regulates primexine deposition, accumulated abnormally at the TGN/EE in ap1σ1 mutants. We show that AP‐1μ recognizes the YXXΦ motif of RPG1, thereby regulating its PM abundance through endocytic trafficking, and that loss of AP1σ1 decreases the levels of other AP‐1 subunits at the TGN/EE.Our observations show that AP‐1‐mediated post‐Golgi trafficking plays a vital role in pollen wall development by regulating protein transport in tapetal cells and microspores.

Slow development allows redundant genes to restore the fertility of rpg1, a TGMS line in Arabidopsis.

Slow development has been shown to be a general mechanism to restore the fertility of thermo-sensitive and photoperiod-sensitive genic male sterile (TGMS and PGMS) lines in Arabidopsis. rpg1 is a TGMS line defective in primexine, which is essential for pollen wall pattern formation. Here, we showed that RPG1-GFP was highly expressed in microsporocytes, microspores, and pollen grains but not in the tapetum in the complemented transgenic line, suggesting that microsporocytes are the main sporophytic cells for primexine formation. Further cytological observations showed that primexine formation in rpg1 was partially restored under slow growth conditions, leading to its fertility restoration. RPG2 is the homolog of RPG1 in Arabidopsis. We revealed that the fertility recovery of rpg1 rpg2 was significantly reduced compared with that of rpg1 under low temperature. The RPG2-GFP protein was also expressed in microsporocytes in the RPG2-GFP (WT) transgenic line. These results suggest that RPG2 plays a redundant role in rpg1 fertility restoration. rpg1 plants were male sterile at the early growth stage, while their fertility was partially restored at the late developmental stage. The fertility of the rpg1 lateral branches was also partially restored. Further growth analysis showed that slow growth at the late reproductive stage or on the lateral branches led to fertility restoration. This work reveals the importance of gene redundancy in fertility restoration for TGMS lines and provides further insight into pollen wall pattern formation.

DCET1 Controls Male Sterility Through Callose Regulation, Exine Formation, and Tapetal Programmed Cell Death in Rice.

In angiosperms, anther development comprises of various complex and interrelated biological processes, critically needed for pollen viability. The transitory callose layer serves to separate the meiocytes. It helps in primexine formation, while the timely degradation of tapetal cells is essential for the timely callose wall dissolution and pollen wall formation by providing nutrients for pollen growth. In rice, many genes have been reported and functionally characterized that are involved in callose regulation and pollen wall patterning, including timely programmed cell death (PCD) of the tapetum, but the mechanism of pollen development largely remains ambiguous. We identified and functionally characterized a rice mutant dcet1, having a complete male-sterile phenotype caused by defects in anther callose wall, exine patterning, and tapetal PCD. DCET1 belongs to the RNA recognition motif (RRM)-containing family also called as the ribonucleoprotein (RNP) domain or RNA-binding domain (RBD) protein, having single-nucleotide polymorphism (SNP) substitution from G (threonine-192) to A (isoleucine-192) located at the fifth exon of LOC_Os08g02330, was responsible for the male sterile phenotype in mutant dcet1. Our cytological analysis suggested that DCET1 regulates callose biosynthesis and degradation, pollen exine formation by affecting exine wall patterning, including abnormal nexine, collapsed bacula, and irregular tectum, and timely PCD by delaying the tapetal cell degeneration. As a result, the microspore of dcet1 was swollen and abnormally bursted and even collapsed within the anther locule characterizing complete male sterility. GUS and qRT-PCR analysis indicated that DCET1 is specifically expressed in the anther till the developmental stage 9, consistent with the observed phenotype. The characterization of DCET1 in callose regulation, pollen wall patterning, and tapetal cell PCD strengthens our knowledge for knowing the regulatory pathways involved in rice male reproductive development and has future prospects in hybrid rice breeding.

Dynamic changes in primexine during the tetrad stage of pollen development.

Formation of pollen wall exine is preceded by the development of several transient layers of extracellular materials deposited on the surface of developing pollen grains. One such layer is primexine (PE), a thin, ephemeral structure that is present only for a short period of time and is difficult to visualize and study. Recent genetic studies suggested that PE is a key factor in the formation of exine, making it critical to understand its composition and the dynamics of its formation. In this study, we used high-pressure frozen/freeze-substituted samples of developing Arabidopsis (Arabidopsis thaliana) pollen for a detailed transmission electron microscopy analysis of the PE ultrastructure throughout the tetrad stage of pollen development. We also analyzed anthers from wild-type Arabidopsis and three mutants defective in PE formation by immunofluorescence, carefully tracing several carbohydrate epitopes in PE and nearby anther tissues during the tetrad and the early free-microspore stages. Our analyses revealed likely sites where these carbohydrates are produced and showed that the distribution of these carbohydrates in PE changes significantly during the tetrad stage. We also identified tools for staging tetrads and demonstrate that components of PE undergo changes resembling phase separation. Our results indicate that PE behaves like a much more dynamic structure than has been previously appreciated and clearly show that Arabidopsis PE creates a scaffolding pattern for formation of reticulate exine.

Loss of THIN EXINE2 disrupts multiple processes in the mechanism of pollen exine formation.

Exine, the sporopollenin-based outer layer of the pollen wall, forms through an unusual mechanism involving interactions between two anther cell types: developing pollen and tapetum. How sporopollenin precursors and other components required for exine formation are delivered from tapetum to pollen and assemble on the pollen surface is still largely unclear. Here, we characterized an Arabidopsis (Arabidopsis thaliana) mutant, thin exine2 (tex2), which develops pollen with abnormally thin exine. The TEX2 gene (also known as REPRESSOR OF CYTOKININ DEFICIENCY1 (ROCK1)) encodes a putative nucleotide-sugar transporter localized to the endoplasmic reticulum. Tapetal expression of TEX2 is sufficient for proper exine development. Loss of TEX2 leads to the formation of abnormal primexine, lack of primary exine elements, and subsequent failure of sporopollenin to correctly assemble into exine structures. Using immunohistochemistry, we investigated the carbohydrate composition of the tex2 primexine and found it accumulates increased amounts of arabinogalactans. Tapetum in tex2 accumulates prominent metabolic inclusions which depend on the sporopollenin polyketide biosynthesis and transport and likely correspond to a sporopollenin-like material. Even though such inclusions have not been previously reported, we show mutations in one of the known sporopollenin biosynthesis genes, LAP5/PKSB, but not in its paralog LAP6/PKSA, also lead to accumulation of similar inclusions, suggesting separate roles for the two paralogs. Finally, we show tex2 tapetal inclusions, as well as synthetic lethality in the double mutants of TEX2 and other exine genes, could be used as reporters when investigating genetic relationships between genes involved in exine formation.

Development of the permanent tetrad wall in Juncus L. (Juncaceae, Poales).

Juncaceae, a cosmopolitan family, belong to the cyperid clade of Poales together with Cyperaceae and Thurniaceae. Pollen grain of Juncaceae, as in Thurniaceae, is dispersed in a permanent tetrad, and knowledge about the ontogeny of its wall is still incipient, based on data from only one species. This study aims to analyze the formation of the pollen wall of seven Juncus species in order to characterize the timing and the ontogenetic events that lead to the cohesion of the four pollen grains in a permanent tetrad. Anthers at different developmental stages were submitted to techniques of light microscopy and transmission electron microscopy; dehiscent anthers with mature pollens were also analyzed in scanning electron microscopy. In all the species here studied, callose deposits around each microsporocyte, with dissolution prior to meiosis. Microspore wall starts at the end of the second meiotic division with formation of primexine. Exine comprises tectum, columellae, and foot layer. During cytokinesis, cell plates form the internal wall of the pollen tetrad. Mature permanent tetrad is enveloped externally by both the exine and intine and internally by the intine and the foot layer, which forms the continuous internal wall. Callose was detected in the early stages of microsporocytes, although reported to be absent in Juncaceae. Our data confirm the variation in Juncaceae cytokinesis and the occurrence of simple cohesion due to the presence of a continuous tectum along the pollen tetrad.

Defective Microspore Development1 is required for microspore cell integrity and pollen wall formation in rice.

Highly coordinated pollen wall patterning is essential for male reproductive development. Here, we report the identification of Defective Microspore Development1 (DMD1), which encodes a nuclear-localized protein possessing transactivation activity. DMD1 is preferentially expressed in the tapetum and microspores during post-meiotic development. Mutations in DMD1 cause a male-sterile phenotype with impaired microspore cell integrity. The mutants display abnormal callose degradation, accompanied by inhibited primexine thickening in the newly released microspores. Several genes associated with callose degradation and primexine formation are downregulated in dmd1 anthers. In addition, irregular Ubisch body morphology and discontinuous endexine occur, and the baculum is completely absent in dmd1. DMD1 interacts with Tapetum Degeneration Retardation (TDR), a basic helix-loop-helix transcription factor required for exine formation. Taken together, our results suggest that DMD1 is responsible for microspore cell integrity, primexine formation and exine pattern formation during Oryza sativa (rice) microspore development.

NERD1 is required for primexine formation and plasma membrane undulation during microsporogenesis in Arabidopsis thaliana.

The primexine formation and plasma membrane undulation are the crucial steps of pollen wall formation in many angiosperms. However, the molecular mechanism underlining these processes is largely unknown. In Arabidopsis, NEW ENHANCER OF ROOT DWARFISM1 (NERD1), a transmembrane protein, was reported to play pleiotropic roles in plant development including male fertility control; while, how NERD1 disruption impacts male reproduction is yet unclear. Here, we revealed that the male sterility of nerd1 mutants is attributed to defects in early steps of pollen wall formation. We found that nerd1-2 is void of primexine formation and microspore plasma membrane undulation, defective in callose deposition. Consequently, sporopollenin precursors are unable to deposit and assemble on the microspore surface, but instead accumulated in the anther locule and tapetal cells, and ultimately leading to microspore abortion. NERD1 is localized in the Golgi and is expressed in both vegetative and reproductive organs, with the highest expression in reproductive tissues, including the tapetum, male meiocytes, tetrads and mature pollen grains. Our results suggest that NERD1 is required for the primexine deposition and microspore plasma membrane undulation, thus essential for sporopollenin assembly and pollen exine formation.

Defective Pollen Wall 3 (DPW3), a novel alpha integrin-like protein, is required for pollen wall formation in rice.

In flowering plants, pollen wall is a specialized extracellular cell-wall matrix surrounding male gametophytes and acts as a natural protector of pollen grains against various environmental and biological stresses. The formation of pollen wall is a complex but well-regulated process, which involves the action of many different genes. However, the genetic and molecular mechanisms underlying this process remain largely unknown. In this study, we isolated and characterized a novel rice male sterile mutant, defective pollen wall3 (dpw3), which displays smaller and paler anthers with aborted pollen grains. DPW3 encodes a novel membrane-associated alpha integrin-like protein conserved in land plants. DPW3 is ubiquitously expressed in anther developmental stages and its protein is localized to the plasma membrane, endoplasmic reticulum (ER) and Golgi. Anthers of dpw3 plants exhibited unbalanced anther cuticular profile, abnormal Ubisch bodies, disrupted callose deposition, defective pollen wall formation such as abnormal microspore plasma membrane undulation and defective primexine formation, resulting in pollen abortion and complete male sterility. Our findings revealed a novel and vital role of alpha integrin-like proteins in plant male reproduction.

ACOS5 is required for primexine formation and exine pattern formation during microsporogenesis in Arabidopsis

Pollen exine, mainly composed of sporopollenin, plays important roles during microspore development. It has been reported that Acyl-CoA Synthetase5 (ACOS5) is required for sporopollenin biosynthesis in Arabidopsis. Here we show that ACOS5 is essential for primexine formation during Arabidopsis microspore development. Through genetic screen, we identified a point mutation of ACOS5 allele, acos5-2, showing abnormal microspore development. Its microspores were degenerated and aborted after released from the tetrads. Transmission electron microscopy showed that primexine formation was reduced in acos5-2 mutant as compared to that of the wild-type. Consequently, sporopollenin was aggregated and randomly deposited on the microspores. In situ hybridization indicated that the key regulators of tapetum development, DYT1 and TDF1, are required for the expression of ACOS5 in tapetum. Furthermore, the GUS reporter showed that the 593-bp promoter sequence was sufficient for the expression of ACOS5 in the anther. Our data provide evidence that ACOS5 is required for primexine formation and sporopollenin deposition during microspore development.

Role of Glycosyltransferases in Pollen Wall Primexine Formation and Exine Patterning

The pollen cell wall is important for protection of male sperm from physical stresses and consists of an inner gametophyte-derived intine layer and a sporophyte-derived exine layer. The polymeric constituents of the robust exine are termed sporopollenin. The mechanisms by which sporopollenin is anchored onto microspores and polymerized in specific patterns are unknown, but the primexine, a transient cell wall matrix formed on the surface of microspores at the late tetrad stage, is hypothesized to play a key role. Arabidopsis (Arabidopsis thaliana) spongy (spg) and uneven pattern of exine (upex) mutants exhibit defective and irregular exine patterns. SPG2 (synonymous with IRREGULAR XYLEM9-LIKE [IRX9L]) encodes a family GT43 glycosyltransferase involved in xylan backbone biosynthesis, while UPEX1 encodes a family GT31 glycosyltransferase likely involved in galactosylation of arabinogalactan proteins. Imaging of developing irx9l microspores showed that the earliest detectable defect was in primexine formation. Furthermore, wild-type microspores contained primexine-localized epitopes indicative of the presence of xylan, but these were absent in irx9l These data, together with the spg phenotype of a mutant in IRX14L, which also plays a role in xylan backbone elongation, indicate the presence of xylan in pollen wall primexine, which plays a role in exine patterning on the microspore surface. We observed an aberrant primexine and irregular patterns of incipient sporopollenin deposition in upex1, suggesting that primexine-localized arabinogalactan proteins could play roles in sporopollenin adhesion and patterning early in microspore wall development. Our data provide new insights into the biochemical and functional properties of the primexine component of the microspore cell wall.

Premature breakdown of tapetum associated with reverse thermo-sensitive genic male-sterile line Huiyou50S in rapeseed (Brassica napus)

Thermo-sensitive genic male-sterility (TGMS) has great advantages in hybrid crop production. Different from common TGMS in Brassica napus, a reverse TGMS line named Huiyou50S is male sterile when it is cultivated in low temperature, but highly fertile when exposed to high temperature. To gain further insights into the developmental aberrations leading to this male sterility, the anther development of Huiyou50S was observed by light and electron microscopy. Firstly, it was suggested by light microscopy that the abortion of anther occurred at the tetrad to early uninucleate microspore stage. A premature breakdown of tapetum is associated with protoplast degradation in the uninucleate microspores. Under transmission electron microscope, the tapetum exhibited vacuolization from pollen mother cell (PMC) stage to tetrad microspore stage and was then disrupted before late microspore stage. Alterations in the tapetal cells included abnormal plastids and a loss of recognizable elaioplast. However, the endoplasmic reticulum seemed to be normal as in the fertile plant. The formation of primexine on the surface of tetrad microspores was postponed to the uninucleate microspore, and hence exine construction was delayed. The evidences suggested that a premature breakdown of tapetum characterized by vacuolization, less secretory activity and abnormal elaioplast, rather than programmed cell death in normal plant, was associated with microspore abortion in Huiyou50S.

The Arabidopsis Exine Formation Defect (EFD) gene is required for primexine patterning and is critical for pollen fertility

Exine, the outermost layer of a pollen grain, has important roles in protecting microspore cytoplasm and determining species-specific interactions between pollen and stigma. The molecular mechanism underlying pollen exine formation, however, remains largely unknown. Here, we report the characterization of an Arabidopsis male-sterile mutant, efd, which exhibits male sterility in first-forming flowers. The Exine Formation Defect (EFD) gene is strongly expressed in microsporocytes, tetrads and the tapetum, and encodes a nuclear-localized de novo DNA methyltransferase. Detailed observations revealed that EFD is involved in both callose wall and primexine formation during microsporogenesis. Microspores in tetrads are not well separated in efd due to an abnormal callose wall. Its plasma membrane undulation appears normal, but primexine patterning is impaired. Primexine matrix establishment and sporopollenin accumulation at specific positions are disturbed, and thus exine formation is totally blocked in efd. We confirmed that EFD is required for pollen exine formation and male fertility via the regulation of callose wall and primexine formation. We also found that positional sporopollenin accumulation is not involved in regulating membrane undulation, but is related to the complete separation of tetrad microspores during primary exine patterning.

AUXIN RESPONSE FACTOR17 Is Essential for Pollen Wall Pattern Formation in Arabidopsis

In angiosperms, pollen wall pattern formation is determined by primexine deposition on the microspores. Here, we show that AUXIN RESPONSE FACTOR17 (ARF17) is essential for primexine formation and pollen development in Arabidopsis (Arabidopsis thaliana). The arf17 mutant exhibited a male-sterile phenotype with normal vegetative growth. ARF17 was expressed in microsporocytes and microgametophytes from meiosis to the bicellular microspore stage. Transmission electron microscopy analysis showed that primexine was absent in the arf17 mutant, which leads to pollen wall-patterning defects and pollen degradation. Callose deposition was also significantly reduced in the arf17 mutant, and the expression of CALLOSE SYNTHASE5 (CalS5), the major gene for callose biosynthesis, was approximately 10% that of the wild type. Chromatin immunoprecipitation and electrophoretic mobility shift assays showed that ARF17 can directly bind to the CalS5 promoter. As indicated by the expression of DR5-driven green fluorescent protein, which is an synthetic auxin response reporter, auxin signaling appeared to be specifically impaired in arf17 anthers. Taken together, our results suggest that ARF17 is essential for pollen wall patterning in Arabidopsis by modulating primexine formation at least partially through direct regulation of CalS5 gene expression.

Cytochemistry of pollen development in Campsis radicans (L.) Seem. (Bignoniaceae)

In this study, cytochemical staining methods were used to follow the cytochemical modifications of microspore cytoplasm and sporoderm in Campsis radicans (L.) Seem. from tetrad stage to mature pollen. Flower buds were collected at different stages of development, and the anthers were fixed and embedded in Araldite. To make cytochemical observations under light microscope, semithin sections were cut and stained with different dyes. Cytochemical methods provided the opportunity to localize the reserve material in the microspore and pollen cytoplasm, to distinguish the different layers of the sporoderm, and to determine its chemical structure at different developmental stages. Microspore cytoplasm contains variable amounts of proteins, lipids, and insoluble carbohydrates at different stages of microsporogenesis. Sporoderm formation starts at tetrad stage by the formation of primexine and is completed at vacuolated microspore stage by the addition of sporopollenin from tapetum. During the vacuolization and enlargement of the microspores, the structure and the chemical composition of the exine are modified. The endexine becomes chemically different from the ectexine. The ectexine is composed of sporopollenin and a small amount of protein, whereas the endexine is composed of sporopollenin, proteins, and traces of polysaccharides.

Genetic Regulation of Sporopollenin Synthesis and Pollen Exine Development

Pollen acts as a biological protector of male sperm and is covered by an outer cell wall polymer called the exine, which consists of durable sporopollenin. Despite the astonishingly divergent structure of the exine across taxa, the developmental processes of its formation surprisingly do not vary, which suggests the preservation of a common molecular mechanism. The precise molecular mechanisms underlying pollen exine patterning remain highly elusive, but they appear to be dependent on at least three major developmental processes: primexine formation, callose wall formation, and sporopollenin synthesis. Several lines of evidence suggest that the sporopollenin is built up via catalytic enzyme reactions in the tapetum, and both the primexine and callose wall provide an efficient substructure for sporopollenin deposition. Herein, we review the currently accepted understanding of the molecular regulation of sporopollenin biosynthesis and examine unanswered questions regarding the requirements underpinning proper exine pattern formation, as based on genetic evidence.

RUPTURED POLLEN GRAIN1, a Member of the MtN3/saliva Gene Family, Is Crucial for Exine Pattern Formation and Cell Integrity of Microspores in Arabidopsis

During microsporogenesis, the microsporocyte (or microspore) plasma membrane plays multiple roles in pollen wall development, including callose secretion, primexine deposition, and exine pattern determination. However, plasma membrane proteins that participate in these processes are still not well known. Here, we report that a new gene, RUPTURED POLLEN GRAIN1 (RPG1), encodes a plasma membrane protein and is required for exine pattern formation of microspores in Arabidopsis (Arabidopsis thaliana). The rpg1 mutant exhibits severely reduced male fertility with an otherwise normal phenotype, which is largely due to the postmeiotic abortion of microspores. Scanning electron microscopy examination showed that exine pattern formation in the mutant is impaired, as sporopollenin is randomly deposited on the pollen surface. Transmission electron microscopy examination further revealed that the primexine formation of mutant microspores is aberrant at the tetrad stage, which leads to defective sporopollenin deposition on microspores and the locule wall. In addition, microspore rupture and cytoplasmic leakage were evident in the rpg1 mutant, which indicates impaired cell integrity of the mutant microspores. RPG1 encodes an MtN3/saliva family protein that is integral to the plasma membrane. In situ hybridization analysis revealed that RPG1 is strongly expressed in microsporocyte (or microspores) and tapetum during male meiosis. The possible role of RPG1 in microsporogenesis is discussed.

Altered tapetal PCD and pollen wall development in the Arabidopsis ms1 mutant

The Arabidopsis male sterility1 mutation results in mature anthers that are devoid of pollen. Meiosis and early development progress normally; however, after microspore release, the microspore cytoplasm and tapetum become abnormally granular and vacuolated, and degeneration occurs. Pollen wall development is seriously affected; primexine formation within the callose wall appears to occur normally, however, once the callose is degraded, abnormal deposits of electrodense material are detected which result in irregular spike-shaped structures, rather than the characteristic rod-like shape of the wild-type bacula. The internal intine wall is also reduced compared with wild type. TUNEL (terminal deoxynucleotidyl transferase-mediated dUTP nick end labelling) staining and ultrastructural analysis have indicated that programmed cell death (PCD) occurs in the wild-type tapetum after microspore mitosis I. However, no signs of PCD are seen in the ms1 tapetum, where large autophagic vacuoles and mitochondrial swelling suggest that necrotic-based breakdown of the tapetum is occurring in the ms1 mutant rather than the normal, regulated PCD process. After the formation of the large, autophagic vacuole in the tapetum, TUNEL staining is detected in the mutant microspores, indicating that they may go through a PCD-based breakdown as a secondary consequence of the observed tapetal aberrations. Based on these observations, two possible roles for MS1 can be hypothesized; MS1 may function by modifying the transcription of tapetal-specific genes implicated in pollen wall development, which then regulate pollen wall material secretion and in turn wall development and tapetal PCD. Alternatively, the MS1 gene may control tapetal development by directly regulating tapetal PCD and breakdown.

The HKM gene, which is identical to the MS1 gene of Arabidopsis thaliana, is essential for primexine formation and exine pattern formation

A male-sterile mutant of Arabidopsis thaliana was isolated by T-DNA tagging screening. Using transmission electron microscopy analysis, we revealed that the microspores of this mutant did not have normal thick primexine on the microspore at the tetrad stage. Instead, a moderately electron-dense layer formed around the microspores. Although microspores without normal primexine failed to form a proper reticulate exine pattern at later stages, sporopollenin was deposited and an exine-like hackly structure was observed on the microspores during the microspore stage. Thus, this mutant was named hackly microspore (hkm). It is speculated that the moderately electron-dense layer was primexine, which partially played its role in sporopollenin deposition onto the microspore. Cytological analysis revealed that the tapetum of the hkm mutant was significantly vacuolated, and that vacuolated tapetal cells crushed the microspores, resulting in the absence of pollen grains within the anther at anthesis. Single nucleotide polymorphism analysis demonstrated that the hkm mutation exists within the MS1 gene, which has been reportedly expressed within the tapetum. Our results suggest that the critical process of primexine formation is under sporophytic control .

I ntroduction

BioTechniquesVol. 34, No. 3S IntroductionOpen AccessIntroductionMichael F. Ochs & Andrew K. GodwinMichael F. OchsSearch for more papers by this author & Andrew K. GodwinSearch for more papers by this authorPublished Online:24 Sep 2018https://doi.org/10.2144/mar03introAboutSectionsPDF/EPUB ToolsAdd to favoritesDownload CitationsTrack Citations ShareShare onFacebookTwitterLinkedInReddit "Introduction." , 34(S3), pp. S1–FiguresReferencesRelatedDetailsCited ByACOS5 is required for primexine formation and exine pattern formation during microsporogenesis in Arabidopsis8 August 2017 | Journal of Plant Biology, Vol. 60, No. 4Sources of Clostridia in Raw Milk on FarmsApplied and Environmental Microbiology, Vol. 74, No. 20 Vol. 34, No. 3S Follow us on social media for the latest updates Metrics Downloaded 83 times History Published online 24 September 2018 Published in print March 2003 Information© 2018 Author(s)PDF download