scholarly journals PRX9 and PRX40 are extensin peroxidases essential for maintaining tapetum and microspore cell wall integrity during Arabidopsis anther development

2018 ◽  
Author(s):  
Joseph R. Jacobowitz ◽  
Jing-Ke Weng

AbstractPollen and microspore development is an essential step in the life cycle of all land plants that generate male gametes. Within flowering plants, pollen development occurs inside of the anther. Here, we report the identification of two class III peroxidase-encoding genes, PRX9 and PRX40, that are genetically redundant and essential for proper anther and pollen development in Arabidopsis thaliana. Arabidopsis double mutants devoid of functional PRX9 and PRX40 are male-sterile. The mutant anthers display swollen, hypertrophic tapetal cells and pollen grains, suggesting disrupted cell wall integrity. These phenotypes ultimately lead to nearly 100%-penetrant pollen degeneration upon anther maturation. Using immunochemical and biochemical approaches, we show that PRX9 and PRX40 are likely extensin peroxidases that contribute to the establishment of tapetal cell wall integrity during anther development. This work identifies PRX9 and PRX40 as the first extensin peroxidases to be described in Arabidopsis and highlights the importance of extensin cross-linking during plant development.

1968 ◽  
Vol 3 (2) ◽  
pp. 161-174
Author(s):  
P. ECHLIN ◽  
H. GODWIN

The ontogeny of the tapetum and Ubisch bodies in Helleborus foetidus L. has been examined at the ultrastructural level, and their development has been closely linked with that of the sporogenous cell and pollen grains. During development the tapetum passes through successive phases of synthesis, maturity and senescence, ending in complete dissolution. During the anabolic phase of growth, precursors of the Ubisch bodies are formed as spheroidal vesicles of medium electron density within the tapetal cytoplasm; they are associated with a zone of radiating ribosomes, which, as development proceeds, can clearly be seen to be situated on strands of endoplasmic reticulum. The callose special wall round the microspores and the tapetal cell wall now disintegrate and the pro-Ubisch bodies are extruded through the cell membrance of the tapetal cells, where they remain on the surface of the anther cavity and soon become irregularly coated with sporopollenin. Deposition of sporopollenin continues on the Ubisch bodies at the same time as upon the exines of the developing pollen grains. In both cases, the later stages of sporopollenin deposition are associated with electron-transparent layers of unit-membrane dimensions appearing in section as white lines of uniform thickness. Continuing deposition of sporopollenin leads to the formation of compound or aggregate Ubisch bodies. It is conjectured that the sporopollenin is synthesized from the compounds of low molecular weight released into the anther loculus by the breakdown of the callose special wall and the tapetal cell wall. The final stages of tapetal autolysis involve the disappearance of all the cell organelles. An attempt is made to relate the findings to those described in other recent studies on Ubisch body formation and to combine them in a common ontogenetic pattern.


2020 ◽  
Vol 61 (5) ◽  
pp. 988-1004 ◽  
Author(s):  
Xiaoying Pan ◽  
Wei Yan ◽  
Zhenyi Chang ◽  
Yingchao Xu ◽  
Ming Luo ◽  
...  

Abstract Pollen development is critical to the reproductive success of flowering plants, but how it is regulated is not well understood. Here, we isolated two allelic male-sterile mutants of OsMYB80 and investigated how OsMYB80 regulates male fertility in rice. OsMYB80 was barely expressed in tissues other than anthers, where it initiated the expression during meiosis, reached the peak at the tetrad-releasing stage and then quickly declined afterward. The osmyb80 mutants exhibited premature tapetum cell death, lack of Ubisch bodies, no exine and microspore degeneration. To understand how OsMYB80 regulates anther development, RNA-seq analysis was conducted to identify genes differentially regulated by OsMYB80 in rice anthers. In addition, DNA affinity purification sequencing (DAP-seq) analysis was performed to identify DNA fragments interacting with OsMYB80 in vitro. Overlap of the genes identified by RNA-seq and DAP-seq revealed 188 genes that were differentially regulated by OsMYB80 and also carried an OsMYB80-interacting DNA element in the promoter. Ten of these promoter elements were randomly selected for gel shift assay and yeast one-hybrid assay, and all showed OsMYB80 binding. The 10 promoters also showed OsMYB80-dependent induction when co-expressed in rice protoplast. Functional annotation of the 188 genes suggested that OsMYB80 regulates male fertility by directly targeting multiple biological processes. The identification of these genes significantly enriched the gene networks governing anther development and provided much new information for the understanding of pollen development and male fertility.


2019 ◽  
Vol 71 (6) ◽  
pp. 1943-1955 ◽  
Author(s):  
Ziyi Cheng ◽  
Xiaorui Guo ◽  
Jiaxue Zhang ◽  
Yadi Liu ◽  
Bing Wang ◽  
...  

Abstract Vacuolar processing enzyme (VPE) is responsible for the maturation and activation of vacuolar proteins in plants. We found that βVPE was involved in tapetal degradation and pollen development by transforming proproteases into mature protease in Arabidopsis thaliana. βVPE was expressed specifically in the tapetum from stages 5 to 8 of anther development. The βVPE protein first appeared as a proenzyme and was transformed into the mature enzyme before stages 7–8. The recombinant βVPE protein self-cleaved and transformed into a 27 kDa mature protein at pH 5.2. The mature βVPE protein could induce the maturation of CEP1 in vitro. βvpe mutants exhibited delayed vacuolar degradation and decreased pollen fertility. The maturation of CEP1, RD19A, and RD19C was seriously inhibited in βvpe mutants. Our results indicate that βVPE is a crucial processing enzyme that directly participates in the maturation of cysteine proteases before vacuolar degradation, and is indirectly involved in pollen development and tapetal cell degradation.


HortScience ◽  
2020 ◽  
Vol 55 (6) ◽  
pp. 945-950
Author(s):  
Weiping Zhong ◽  
Zhoujun Zhu ◽  
Fen Ouyang ◽  
Qi Qiu ◽  
Xiaoming Fan ◽  
...  

The normal development of anthers and the formation of functional pollen are the prerequisites for successful pollination and fertilization. In this study, we observed dynamic changes in inflorescence and anther development in the chinquapin (Castanea henryi) using stereomicroscopy, light microscopy, and transmission electron microscopy. We found that cytokinesis during meiosis in microsporocytes was of the simultaneous type, and that the tetrads were mainly tetrahedral. Mature pollen grains contained two cells with three germ pores. The anther wall was of the basic type and composed of epidermis, endothecium, middle layers, and tapetum. Mature anthers had no middle layer and tapetum. The tapetum was of the glandular type. At the early microspore stage, a large number of starch granules appeared in the endothecium, which was deformed at the late microspore stage. Lipid droplets appeared in tapetum during the early microspore stage, and a few lipid droplets were still found during tapetum degeneration. The mature pollen accumulated a large amount of starch and lipids. These findings demonstrated that the anther wall provides nutrients and protection for pollen development. There is relatively stable correspondence between the external morphological characteristics of male flowers and internal structure of anther development.


2018 ◽  
Author(s):  
Ziyi Cheng ◽  
Bin Yin ◽  
Jiaxue Zhang ◽  
Yadi Liu ◽  
Bing Wang ◽  
...  

Vacuolar processing enzyme (VPE) is responsible for the maturation and activation of vacuolar proteins in plants. We found that βVPE was involved in tapetal degradation and pollen development by transforming proproteases into mature protease in Arabidopsis thaliana. βVPE was expressed specifically in the tapetum from stages 5–8 of anther development. The βVPE protein first appeared as a proenzyme and transformed into the mature enzyme before stages 7–8. The recombinant βVPE protein self-cleaved and transformed to a 27-kD mature protein at pH 5.2. The mature βVPE protein could induce the maturation of CEP1 in vitro. βvpe mutants exhibited delayed vacuolar degradation and decreased pollen fertility. The maturation of CEP1, RD19A, and RD19C were seriously inhibited in βvpe mutants. Our results indicate that βVPE is a crucial processing enzyme that directly participates in the maturation of cysteine proteases before vacuolar degradation, and is indirectly involved in pollen development and tapetal cell degradation.


2021 ◽  
Vol 12 ◽  
Author(s):  
Xinyue Liu ◽  
Ze Wu ◽  
Jingxian Feng ◽  
Guozhen Yuan ◽  
Ling He ◽  
...  

Lily (Lilium spp.) is an important commercial flower crop, but its market popularity and applications are adversely affected by severe pollen pollution. Many studies have examined pollen development in model plants, but few studies have been conducted on flower crops such as lily. GAMYBs are a class of R2R3-MYB transcription factors and play important roles in plant development and biotic resistance; their functions vary in different pathways, and many of them are involved in anther development. However, their function and regulatory role in lily remain unclear. Here, the GAMYB homolog LoMYB33 was isolated and identified from lily. The open reading frame of LoMYB33 was 1620 bp and encoded a protein with 539 amino acids localized in the nucleus and cytoplasm. Protein sequence alignment showed that LoMYB33 contained a conserved R2R3 domain and three BOX motifs (BOX1, BOX2, and BOX3), which were unique to the GAMYB family. LoMYB33 had transcriptional activation activity, and its transactivation domain was located within 90 amino acids of the C-terminal. LoMYB33 was highly expressed during the late stages of anther development, especially in pollen. Analysis of the promoter activity of LoMYB33 in transgenic Arabidopsis revealed that the LoMYB33 promoter was highly activated in the pollen of stage 12 to 13 flowers. Overexpression of LoMYB33 in Arabidopsis significantly retarded growth; the excess accumulation of LoMYB33 also negatively affected normal anther development, which generated fewer pollen grains and resulted in partial male sterility in transgenic plants. Silencing of LoMYB33 in lily also greatly decreased the amount of pollen. Overall, our results suggested that LoMYB33 might play an important role in the anther development and pollen formation of lily.


2018 ◽  
Author(s):  
Wympher Langstang ◽  
Eros Kharshiing ◽  
Nagulan Venugopal

AbstractGaultheria fragrantissima Wall. (Ericaceae) is a gynodioecious species having both hermaphrodite and male sterile plants. In this study, we present a comparative analysis of the different stages of anther development in naturally occuring hermaphrodite and male sterile populations of G. fragrantissima found in Meghalaya, India. While hermaphrodite flowers had well developed anther lobes, the male sterile flowers formed a white unorganized mass of tissues with a tuft of hairy outgrowth at the tip of the stamens. Histological analyses of progressive anther development in both the lines indicate an abnormal development of the sporogenous tissue in the developing anthers in the male steril line. While anther development in the hermaphrodite line was of the dicotyledonous type, the anthers of male sterile line showed progressive degradation of the sporogenous tissues and wall layers. Pollen development was also disrupted in male sterile line resulting in distorted pollen due to the irregular projection of exine wall. Our results suggest that premature degradation of the sporogenous tissues during anther development determines male sterility in G. fragrantissima.


2020 ◽  
Author(s):  
Xinqi Cheng ◽  
Xinyu Zhang ◽  
Fei Xue ◽  
Shouhong Zhu ◽  
Yanjun Li ◽  
...  

Abstract Background : Male sterility is an efficient trait for hybrid seed production and germplasm innovation. Until now, most studies on male sterility were on cytoplasmic and recessive genic sterility, with few on dominant genic male sterility, especially in cotton, due to lack of such mutant.Results : We discovered a natural male sterile (MS) Sea Island cotton ( G. barbadense ) mutant, Genetic analysis showed the mutation was caused by a dominant mutation in a single nuclear gene. Comparative cytological observation of anther sections from MS and WT uncovered cellular differences in anther at and after the tetrad stage of pollen mother cells (PMC). In the MS anthers, the outer wall of pollen grains was free of spinules, the tapetum was vacuolated and showed delayed degradation, consequently, no functional pollen grains. Comparison of transcriptomes from meiosis, tetrad, mononuclear and binuclear pollen, and pollen maturation stages identified 13,783 non-redundant differentially expressed genes (DEGs) between MS and WT. Based on the number of DEGs, analyses of enriched GO terms and KEGG pathways, it was evident that significant transcriptomic changes occurred at and after the tetrad stage, consistent with cytological observation, and that the major differences were on metabolism of starch, sucrose, ascorbate, aldarate, alanine, aspartate and glutamate, and biosynthesis of cutin, suberine and wax. WGCNA analysis identified five modules containing 920 genes highly related to anther development, especially the greenyellow module with 54 genes that was highly associated with PMC meiosis and tetrad formation. A NAC transcription factor ( Gh_D11G2469 ) was identified as a hub gene for this module, which warrants further functional characterization.Conclusions : We demonstrated that the MS trait was controlled by a single dominant nuclear gene and caused by delayed tapetum degradation at the tetrad stage. Comparative transcriptome analysis and gene network construction identified DEGs, enriched GO terms and metabolic pathways, and hub genes potentially associated with anther development and the MS trait, which will contribute to important ideas and basis of the experimental data related to the molecular mechanism of DGMS and the innovation of cotton germplasm resources.


2019 ◽  
Author(s):  
Jens Westermann ◽  
Susanna Streubel ◽  
Christina Maria Franck ◽  
Roswitha Lentz ◽  
Liam Dolan ◽  
...  

AbstractRooting cells and pollen tubes – key adaptative innovations that evolved during the colonization and subsequent radiation of plants on land – expand by tip-growth. Tip-growth relies on a tight coordination between the protoplast growth and the synthesis/remodeling of the external cell wall. In root hairs and pollen tubes of the seed plant Arabidopsis thaliana, cell wall integrity (CWI) mechanisms monitor this coordination through the Malectin-like receptor kinases (MLRs) such as AtANXUR1 and AtFERONIA that act upstream of the AtMARIS PTI1-like kinase. Here, we show that rhizoid growth in the early diverging plant, Marchantia polymorpha, is also controlled by an MLR and PTI1-like signaling module. Rhizoids, root hairs and pollen tubes respond similarly to disruption of MLR and PTI1-like encoding genes. Thus, the MLR/PTI1-like signaling module that controls CWI during tip-growth is conserved between M. polymorpha and A. thaliana suggesting it was active in the common ancestor of land plants.


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