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.

Genetic Regulation of Sporopollenin Synthesis and Pollen Exine Development

In plants, male reproductive development is extremely sensitive to adverse climatic environments and (a)biotic stress. Upon exposure to stress, male gametophytic organs often show morphological, structural and metabolic alterations that typically lead to meiotic defects or premature spore abortion and male reproductive sterility. Depending on the type of stress involved (e.g. heat, cold, drought) and the duration of stress exposure, the underlying cellular defect is highly variable and either involves cytoskeletal alterations, tapetal irregularities, altered sugar utilization, aberrations in auxin metabolism, accumulation of reactive oxygen species (ROS; oxidative stress) or the ectopic induction of programmed cell death (PCD). In this review, we present the critically stress-sensitive stages of male sporogenesis (meiosis) and male gametogenesis (microspore development), and discuss the corresponding biological processes involved and the resulting alterations in male reproduction. In addition, this review also provides insights into the molecular and/or hormonal regulation of the environmental stress sensitivity of male reproduction and outlines putative interaction(s) between the different processes involved.

https://biblio.ugent.be/publication/4110545/file/4110547.pdf

The impact of environmental stress on male reproductive development in plants: biological processes and molecular mechanisms.

The regulation of protein expression and activity has been for long time considered only in terms of transcription/translation efficiency. In the last years, the discovery of post-transcriptional and post-translational regulation mechanisms pointed out that the key factor in determining transcript/protein amount is the synthesis/degradation ratio, together with post-translational modifications of proteins. Polyubiquitinaytion marks target proteins directed to degradation mediated by 26S-proteasome. Recent functional genomics studies pointed out that about 5% of Arabidopsis genome codes for proteins of ubiquitination pathway. The most of them (more than one thousand genes) correspond to E3 ubiquitin ligases that specifically recognise target proteins. The huge size of this gene family, whose members are involved in regulation of a number of biological processes including hormonal control of vegetative growth, plant reproduction, light response, biotic and abiotic stress tolerance and DNA repair, indicates a major role for protein degradation in control of plant life.

The e3 ubiquitin ligase gene family in plants: regulation by degradation.

The Arabidopsis basic helix-loop-helix (bHLH) proteins INDEHISCENT (IND) and ALCATRAZ (ALC) specify tissues required for fruit opening that have major roles in seed dispersal and plant domestication. Here, we show that synthesis of the phytohormone gibberellin is a direct and necessary target of IND, and that ALC interacts directly with DELLA repressors, which antagonize ALC function but are destabilized by gibberellin. Thus, the gibberellin/DELLA pathway has a key role in patterning the Arabidopsis fruit, and the interaction between DELLA and bHLH proteins, previously shown to connect gibberellin and light responses, is a versatile regulatory module also used in tissue patterning.

/pdf/gibberellins-control-fruit-patterning-in-arabidopsis-yss1w0xw53.pdf

Gibberellins control fruit patterning in Arabidopsis thaliana

In flowering plants, the tapetum, the innermost layer of the anther, provides both nutrient and lipid components to developing microspores, pollen grains, and the pollen coat. Though the programmed cell death of the tapetum is one of the most critical and sensitive steps for fertility and is affected by various environmental stresses, its regulatory mechanisms remain mostly unknown. Here we show that autophagy is required for the metabolic regulation and nutrient supply in anthers and that autophagic degradation within tapetum cells is essential for postmeiotic anther development in rice. Autophagosome-like structures and several vacuole-enclosed lipid bodies were observed in postmeiotic tapetum cells specifically at the uninucleate stage during pollen development, which were completely abolished in a retrotransposon-insertional OsATG7 (autophagy-related 7)-knockout mutant defective in autophagy, suggesting that autophagy is induced in tapetum cells. Surprisingly, the mutant showed complete sporophytic ma...

https://www.tandfonline.com/doi/pdf/10.4161/auto.28279

OsATG7 is required for autophagy-dependent lipid metabolism in rice postmeiotic anther development

INDEHISCENT (IND) is one of the major factors of a transcriptional network regulating fruit dehiscence in Arabidopsis thaliana. However, partially owing to the lack of knowledge on the morphogenic process at the junction between the valve margin and the replum, the cellular processes regulated by IND have not been elucidated. Here we report the identification of a zone of seven layers of cells relevant to silique dehiscence, and the isolation and characterization of a transposon-enhancer-trap-generated null allele of IND, ind-6. Light microscopy analysis revealed that the β-glucuronidase from the enhancer trap was expressed in a seven-layer zone, encompassing the valve margin and the replum border. Electron and light microscopy analyses also revealed that unequal cell divisions actively occurred at stage 15 in the seven-layer zone in wild type (WT), which apparently produced the distinct cell types in the WT seven-layer zone. In contrast, siliques of ind-6 at stage 15 did not exhibit such cell divisions but fewer cells and defective cytokinesis, hence lacking the distinct cell types in the seven-layer zone. These results demonstrate a cellular mechanism for establishing the distinct cell types and a role for IND in regulating the unequal cell divisions in the seven-layer zone.

The INDEHISCENT protein regulates unequal cell divisions in Arabidopsis fruit.

The migration of nucleolus to the nuclear periphery and the onset of homologous chromosome synapsis are characteristics of the leptotene to zygotene transition in meiocytes Little is known about the genes regulating these processes in eukaryotes Here we report the characterization of morphological defects in prophase I in microsporocytes in the Arabidopsis skp1-like1 (ask1-1) mutant In ask1-1, the nucleolus of the microsporocyte failed to move to the nuclear periphery throughout prophase I, and the chromosomes failed to synapse, despite the formation of bivalents in late prophase I We also found that the transcription of the DMC1 gene and ASY1 gene, which were predominantly transcribed prior to zygotene in microsporocytes, was not affected in ask1-1 These findings, and the fact that ASK1 is a component of the SCF ubiquitin ligase, suggest that ASK1 regulates either the leptotene to zygotene transition or events associated with the developmental transition during male meiosis in Arabidopsis

Defects in nucleolar migration and synapsis in male prophase I in the ask1-1 mutant of Arabidopsis

Although the tapetum is known for its role in the removal of the tetrad wall, a morphological change in the tapetum correlating with such a role has not been described. Here we report that in two ecotypes of Arabidopsis thaliana, Landsberg erecta and Columbia, the vacuoles in tapetal cells underwent progressive enlargement prior to the separation of tetrads but became drastically reduced when tetrads just separated from one another. Such a drastic change in vacuolar volume was not observed in later anther development. We also observed that the walls of associated tetrads were much less stained with Toluidine Blue O than the walls of separate tetrads, indicating that the tetrad walls underwent an alteration during the tetrad stage. Furthermore, we identified the N-terminal propeptide signals for sorting vacuolar proteins in 15 β-1,3-glucanases, five polygalacturonases, and two endocellulases that are expressed in Arabidopsis young floral buds; all three types of the enzymes are known to participate in degradation of the tetrad wall. These results suggest that the tapetal vacuoles might be a storage site for these enzymes prior to their secretion to the anther locule.

Hong Wu

Papers

The INDEHISCENT protein regulates unequal cell divisions in Arabidopsis fruit.

Defects in nucleolar migration and synapsis in male prophase I in the ask1-1 mutant of Arabidopsis

Reduction in vacuolar volume in the tapetal cells coincides with conclusion of the tetrad stage in Arabidopsis thaliana

Microscopy and bioinformatic analyses of lipid metabolism implicate a sporophytic signaling network supporting pollen development in Arabidopsis.