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Plant Fertility and Sexual Reproduction

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A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Plant Sciences".

Deadline for manuscript submissions: closed (30 April 2020) | Viewed by 28127

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Prof. Dr. Renate Horn

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Department of Plant Genetics, Institute of Biological Sciences, University of Rostock, Albert-Einstein-Str. 3, 18059 Rostock, Germany
Interests: hybrid breeding; cytoplasmic male sterility; fertility restoration; pollen development; marker-assisted selection; association studies; sunflowers

Special Issue Information

Dear Colleagues,

Fertility is crucial to sexual reproduction in plant species. Cytoplasmic male sterility (CMS) can occur spontaneously or can be induced by interspecific crosses or by mutagenesis. Development of CMS is interesting from the standpoint of population genetics as well as agriculture. In hybrid systems based on CMS, fertility restoration that is achieved mostly by dominant, nuclear-encoded restorer-of-fertility (Rf) genes is essential and the environmental stability as well as the degree of fertility restoration determines its usability for hybrid breeding. CMS is caused by rearrangements of the mitochondrial genome and leads in most cases to new chimeric open reading frames whose products interfere with the normal mitochondrial functions. The CMS/fertility restoration system is ideal for studying the role of mitochondria in pollen development and sexual reproduction. Restorer genes have been divided into two classes: pentatricopeptide repeat (PPR) genes and non-PPR genes. PPR genes represent a large gene family that plays a major role in RNA processing, RNA editing, and RNA stability in mitochondria as well as chloroplasts. Non-PPR genes represent a diverse group of genes that address basic processes to allow for production and shedding of functional pollen. Studying all of these processes has helped us to better understand the interactions between the nucleus and organelles (mitochondria and chloroplasts). In recent years, we have learnt more and more about fertility restoration in different systems and the role of mitochondria in pollen development. However, we are far from having fully identified all functions in the complex co-evolution of these organelles.

The Special Issue “Plant Fertility and Sexual Reproduction” will emphasize the role of restorer-of-fertility genes in the complex interaction between the nucleus and mitochondria in order to realize sexual reproduction.

Prof. Dr. Renate Horn
Guest Editor

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Keywords

fertility restoration
flower development
sexual reproduction
evolution
association studies
functional and mutant analyses

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Published Papers (8 papers)

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Research

14 pages, 2144 KiB

Open AccessArticle

The Mitochondrial Genome Assembly of Fennel (Foeniculum vulgare) Reveals Two Different atp6 Gene Sequences in Cytoplasmic Male Sterile Accessions

by Fabio Palumbo, Nicola Vitulo, Alessandro Vannozzi, Gabriele Magon and Gianni Barcaccia

Int. J. Mol. Sci. 2020, 21(13), 4664; https://doi.org/10.3390/ijms21134664 - 30 Jun 2020

Cited by 11 | Viewed by 3636

Abstract

Cytoplasmic male sterility (CMS) has always aroused interest among researchers and breeders, being a valuable resource widely exploited not only to breed F1 hybrid varieties but also to investigate genes that control stamen and pollen development. With the aim of identifying candidate genes for CMS in fennel, we adopted an effective strategy relying on the comparison between mitochondrial genomes (mtDNA) of both fertile and sterile genotypes. mtDNA raw reads derived from a CMS genotype were assembled in a single molecule (296,483 bp), while a draft mtDNA assembly (166,124 nucleotides, 94 contigs) was performed using male fertile sample (MF) sequences. From their annotation and alignment, two atp6-like sequences were identified. atp6⁻, the putative mutant copy with a 300 bp truncation at the 5’-end, was found only in the mtDNA of CMS samples, while the wild type copy (atp6⁺) was detected only in the MF mtDNA. Further analyses (i.e., reads mapping and Sanger sequencing), revealed an atp6⁺ copy also in CMS samples, probably in the nuclear DNA. However, qPCRs performed on different tissues proved that, despite its availability, atp6⁺ is expressed only in MF samples, while apt6⁻ mRNA was always detected in CMS individuals. In the light of these findings, the energy deficiency model could explain the pollen deficiency observed in male sterile flower. atp6⁻ could represent a gene whose mRNA is translated into a not-fully functional protein leading to suboptimal ATP production that guarantees essential cellular processes but not a high energy demand process such as pollen development. Our study provides novel insights into the fennel mtDNA genome and its atp6 genes, and paves the way for further studies aimed at understanding their functional roles in the determination of male sterility. Full article

(This article belongs to the Special Issue Plant Fertility and Sexual Reproduction)

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14 pages, 7048 KiB

Open AccessArticle

Male sterile 305 Mutation Leads the Misregulation of Anther Cuticle Formation by Disrupting Lipid Metabolism in Maize

by Haichun Shi, Yang Yu, Ronghuan Gu, Chenxi Feng, Yu Fu, Xuejie Yu, Jichao Yuan, Qun Sun and Yongpei Ke

Int. J. Mol. Sci. 2020, 21(7), 2500; https://doi.org/10.3390/ijms21072500 - 3 Apr 2020

Cited by 5 | Viewed by 2754

Abstract

The anther cuticle, which is mainly composed of lipid polymers, functions as physical barriers to protect genetic material intact; however, the mechanism of lipid biosynthesis in maize (Zea mays. L.) anther remains unclear. Herein, we report a male sterile mutant, male sterile 305 (ms305), in maize. It was shown that the mutant displayed a defective anther tapetum development and premature microspore degradation. Three pathways that are associated with the development of male sterile, including phenylpropanoid biosynthesis, biosynthesis of secondary metabolites, as well as cutin, suberine, and wax biosynthesis, were identified by transcriptome analysis. Gas chromatography-mass spectrometry disclosed that the content of cutin in ms305 anther was significantly lower than that of fertile siblings during the abortion stage, so did the total fatty acids, which indicated that ms305 mutation might lead to blocked synthesis of cutin and fatty acids in anther. Lipidome analysis uncovered that the content of phosphatidylcholine, phosphatidylserine, diacylglycerol, monogalactosyldiacylglycerol, and digalactosyldiacylglycerol in ms305 anther was significantly lower when compared with its fertile siblings, which suggested that ms305 mutation disrupted lipid synthesis. In conclusion, our findings indicated that ms305 might affect anther cuticle and microspore development by regulating the temporal progression of the lipidome in maize. Full article

(This article belongs to the Special Issue Plant Fertility and Sexual Reproduction)

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17 pages, 4598 KiB

Open AccessArticle

Comparative Transcriptome Analysis Reveals the Potential Mechanism of Abortion in Tobacco sua-Cytoplasmic Male Sterility

by Zhiwen Liu, Yanfang Liu, Yuhe Sun, Aiguo Yang and Fengxia Li

Int. J. Mol. Sci. 2020, 21(7), 2445; https://doi.org/10.3390/ijms21072445 - 1 Apr 2020

Cited by 12 | Viewed by 3006

Abstract

sua-CMS (cytoplasmic male sterility) is the only male sterile system in tobacco breeding, but the mechanism of abortion is unclear. Cytological characteristics show that abortion in the sua-CMS line msZY occurs before the differentiation of sporogenous cells. In this study, a comparative transcriptomic analysis was conducted on flower buds at the abortion stage of msZY and its male fertile control ZY. A total of 462 differentially expressed genes were identified in msZY and ZY, which were enriched via protein processing in the endoplasmic reticulum (ER), oxidative phosphorylation, photosynthesis, and circadian rhythm-plant by Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analyses. Most genes were downregulated in the ER stress pathway, heat-shock protein family, F1F0-ATPase encoding by the mitochondrial genome, and differentiation of stamens. Genes in the programmed cell death (PCD) pathway were upregulated in msZY. The transcriptome results were consistent with those of qRT-PCR. Ultrastructural and physiological analyses indicted active vacuole PCD and low ATP content in msZY young flower buds. We speculated that PCD and a deficiency in ATP synthesis are essential for the abortion of sua-CMS. This study reveals the potential mechanism of abortion of tobacco sua-CMS. Full article

(This article belongs to the Special Issue Plant Fertility and Sexual Reproduction)

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30 pages, 4553 KiB

Open AccessArticle

The Beta Subunit of Nascent Polypeptide Associated Complex Plays A Role in Flowers and Siliques Development of Arabidopsis thaliana

by Jan Fíla, Božena Klodová, David Potěšil, Miloslav Juříček, Petr Šesták, Zbyněk Zdráhal and David Honys

Int. J. Mol. Sci. 2020, 21(6), 2065; https://doi.org/10.3390/ijms21062065 - 17 Mar 2020

Cited by 8 | Viewed by 4124

Abstract

The nascent polypeptide-associated (NAC) complex was described in yeast as a heterodimer composed of two subunits, α and β, and was shown to bind to the nascent polypeptides newly emerging from the ribosomes. NAC function was widely described in yeast and several information are also available about its role in plants. The knock down of individual NAC subunit(s) led usually to a higher sensitivity to stress. In Arabidopsis thaliana genome, there are five genes encoding NACα subunit, and two genes encoding NACβ. Double homozygous mutant in both genes coding for NACβ was acquired, which showed a delayed development compared to the wild type, had abnormal number of flower organs, shorter siliques and greatly reduced seed set. Both NACβ genes were characterized in more detail—the phenotype of the double homozygous mutant was complemented by a functional NACβ copy. Then, both NACβ genes were localized to nuclei and cytoplasm and their promoters were active in many organs (leaves, cauline leaves, flowers, pollen grains, and siliques together with seeds). Since flowers were the most affected organs by nacβ mutation, the flower buds’ transcriptome was identified by RNA sequencing, and their proteome by gel-free approach. The differential expression analyses of transcriptomic and proteomic datasets suggest the involvement of NACβ subunits in stress responses, male gametophyte development, and photosynthesis. Full article

(This article belongs to the Special Issue Plant Fertility and Sexual Reproduction)

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22 pages, 13608 KiB

Open AccessArticle

Distinct Differentiation Characteristics of Endothelium Determine Its Ability to Form Pseudo-Embryos in Tomato Ovules

by Inna Chaban, Ekaterina Baranova, Neonila Kononenko, Marat Khaliluev and Elena Smirnova

Int. J. Mol. Sci. 2020, 21(1), 12; https://doi.org/10.3390/ijms21010012 - 18 Dec 2019

Cited by 5 | Viewed by 3909

Abstract

The endothelium is an additional cell layer, differentiating from the inner epidermis of the ovule integument. In tomato (Solanum lycopersicum L.), after fertilization, the endothelium separates from integument and becomes an independent tissue developing next to the growing embryo sac. In the absence of fertilization, the endothelium may proliferate and form pseudo-embryo. However, the course of the reorganization of endothelium into pseudo-embryo in tomato ovules is poorly understood. We aimed to investigate specific features of endothelium differentiation and the role of the endothelium in the development of fertilized and unfertilized tomato ovules. The ovules of tomato plants (“YaLF” line), produced by vegetative growth plants of transgenic tomato line expressing the ac gene, encoding chitin-binding protein from Amaranthus caudatus L., were investigated using light and transmission electron microscopy. We showed that in the fertilized ovule of normally developing fruit and in the unfertilized ovule of parthenocarpic fruit, separation of the endothelium from integument occurs via programmed death of cells of the integumental parenchyma, adjacent to the endothelium. Endothelial cells in normally developing ovules change their structural and functional specialization from meristematic to secretory and back to meristematic, and proliferate until seeds fully mature. The secretory activity of the endothelium is necessary for the lysis of dying cells of the integument and provides the space for the growth of the new sporophyte. However, in ovules of parthenocarpic fruits, pseudo-embryo cells do not change their structural and functional organization and remain meristematic, no zone of lysis is formed, and pseudo-embryo cells undergo programmed cell death. Our data shows the key role of the endothelium as a protective and secretory tissue, needed for the normal development of ovules. Full article

(This article belongs to the Special Issue Plant Fertility and Sexual Reproduction)

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21 pages, 9074 KiB

Open AccessArticle

Integrated Methylome and Transcriptome Analysis between the CMS-D2 Line ZBA and Its Maintainer Line ZB in Upland Cotton

by Meng Zhang, Liping Guo, Tingxiang Qi, Xuexian Zhang, Huini Tang, Hailin Wang, Xiuqin Qiao, Bingbing Zhang, Juanjuan Feng, Zhidan Zuo, Ting Li, Kashif Shahzad, Jianyong Wu and Chaozhu Xing

Int. J. Mol. Sci. 2019, 20(23), 6070; https://doi.org/10.3390/ijms20236070 - 2 Dec 2019

Cited by 18 | Viewed by 3303

Abstract

DNA methylation is an important epigenetic modification involved in multiple biological processes. Altered methylation patterns have been reported to be associated with male sterility in some plants, but their role in cotton cytoplasmic male sterility (CMS) remains unclear. Here, integrated methylome and transcriptome analyses were conducted between the CMS-D2 line ZBA and its near-isogenic maintainer line ZB in upland cotton. More methylated cytosine sites (mCs) and higher methylation levels (MLs) were found among the three sequence contexts in ZB compared to ZBA. A total of 4568 differentially methylated regions (DMRs) and 2096 differentially methylated genes (DMGs) were identified. Among the differentially expressed genes (DEGs) associated with DMRs (DMEGs), 396 genes were upregulated and 281 genes were downregulated. A bioinformatics analysis of these DMEGs showed that hyper-DEGs were significantly enriched in the “oxidative phosphorylation” pathway. Further qRT-PCR validation indicated that these hypermethylated genes (encoding the subunits of mitochondrial electron transport chain (ETC) complexes I and V) were all significantly upregulated in ZB. Our biochemical data revealed a higher extent of H₂O₂ production but a lower level of adenosine triphosphate (ATP) synthesis in CMS-D2 line ZBA. On the basis of the above results, we propose that disrupted DNA methylation in ZBA may disrupt the homeostasis of reactive oxygen species (ROS) production and ATP synthesis in mitochondria, triggering a burst of ROS that is transferred to the nucleus to initiate programmed cell death (PCD) prematurely, ultimately leading to microspore abortion. This study illustrates the important role of DNA methylation in cotton CMS. Full article

(This article belongs to the Special Issue Plant Fertility and Sexual Reproduction)

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17 pages, 3807 KiB

Open AccessArticle

Comparative Transcriptome Analysis Reveals the Cause for Accumulation of Reactive Oxygen Species During Pollen Abortion in Cytoplasmic Male-Sterile Kenaf Line 722HA

by Bujin Zhou, Yiding Liu, Zhengxia Chen, Dongmei Liu, Yining Wang, Jie Zheng, Xiaofang Liao and and Ruiyang Zhou

Int. J. Mol. Sci. 2019, 20(21), 5515; https://doi.org/10.3390/ijms20215515 - 5 Nov 2019

Cited by 15 | Viewed by 3191

Abstract

Cytoplasmic male sterility (CMS) is a maternally inherited trait used for hybrid production in plants, a novel kenaf CMS line 722HA was derived from the thermo-sensitive male-sterile mutant ‘HMS’ by recurrent backcrossing with 722HB. The line 722HA has great potential for hybrid breeding in kenaf. However, the underlying molecular mechanism that controls pollen abortion in 722HA remains unclear, thus limiting the full utilization of this line. To understand the possible mechanism governing pollen abortion in 722HA, cytological, transcriptomic, and biochemical analyses were carried out to compare the CMS line 722HA and its maintainer line 722HB. Cytological observations of the microspore development revealed premature degradation of the tapetum at the mononuclear stage, which resulted in pollen dysfunction. The k-means clustering analysis of differentially expressed genes (DEGs) revealed that these genes are related to processes associated with the accumulation of reactive oxygen species (ROS), including electron transport chain, F₁F₀-ATPase proton transport, positive regulation of superoxide dismutase (SOD), hydrogen peroxide catabolic, and oxidation-reduction. Biochemical analysis indicated that ROS-scavenging capability was lower in 722HA than in 722HB, resulting in an accumulation of excess ROS, which is consistent with the transcriptome results. Taken together, these results demonstrate that excessive ROS accumulation may affect the normal development of microspores. Our study provides new insight into the molecular mechanism of pollen abortion in 722HA and will promote further studies of kenaf hybrids. Full article

(This article belongs to the Special Issue Plant Fertility and Sexual Reproduction)

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23 pages, 2748 KiB

Open AccessArticle

Using Transcriptome Analysis to Screen for Key Genes and Pathways Related to Cytoplasmic Male Sterility in Cotton (Gossypium hirsutum L.)

by Yuqing Li, Tengfei Qin, Chunyan Wei, Jialiang Sun, Tao Dong, Ruiyang Zhou, Quanjia Chen and Qinglian Wang

Int. J. Mol. Sci. 2019, 20(20), 5120; https://doi.org/10.3390/ijms20205120 - 16 Oct 2019

Cited by 19 | Viewed by 3650

Abstract

Cotton (Gossypium hirsutum L.) is one of the most important cash crops worldwide. Cytoplasmic male sterility (CMS) is an excellent breeding system for exploitation of heterosis, which has great potential to increase crop yields. To understand the molecular mechanism of CMS in cotton, we compared transcriptome, cytomorphological, physiological and bioinformatics data between the CMS line C2P5A and its maintainer line C2P5B. By using high-throughput sequencing technology, 178,166 transcripts were assembled and 2013 differentially expression genes (DEGs) were identified at three different stages of C2P5A anther development. In this study, we identified DEGs associated with reactive oxygen species (ROS), peroxisomes, aldehyde dehydrogenases (ALDH), cytochrome oxidase subunit VI, and cytochrome P450, and DEGs associated with tapetum development, Jojoba acyl-CoA reductase-related male sterility protein, basic helix-loop-helix (bHLH) and MYB transcription factors. The abnormal expression of one of these genes may be responsible for the CMS C2P5A line. In gene ontology (GO) annotation and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway enrichment, DEGs were mainly related to carbohydrate metabolism, amino acid metabolism, transport and catabolism, and signal transduction. Carbohydrate metabolism provides energy for anther development, starch and sucrose metabolism, fatty acid biosynthesis and metabolism and ascorbate and aldarate metabolism. These results showed that numerous genes and multiple complex metabolic pathways regulate cotton anther development. Weighted correlation network analysis (WGCNA) indicated that three modules, ‘turquoise,’ ‘blue,’ and ‘green,’ were specific for the CMS C2P5A line. The ‘turquoise’ and ‘blue’ modules were mainly related to carbohydrate metabolism, amino acid metabolism, energy metabolism, peroxisomes, pyruvate metabolism as well as fatty acid degradation. The ‘green’ module was mainly related to energy metabolism, carbon metabolism, translation, and lipid metabolism. RNA-sequencing and WGCNA polymerization modules were screened for key genes and pathways related to CMS in cotton. This study presents a new perspective for further research into the metabolic pathways of pollen abortion in the CMS C2P5A line and also provides a theoretical basis for its breeding and production. Full article

(This article belongs to the Special Issue Plant Fertility and Sexual Reproduction)

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