From birth to function: Male gametophyte development in flowering plants (2023)

Table of Contents
Current Opinion in Plant Biology Abstract Introduction Section snippets Asymmetric cell division of the microspores Generative cell and vegetative cell: differing in the nucleus Physiological distinctions: sperm cells are passengers of the vegetative cell Conclusion Funding Declaration of competing interest Acknowledgement References (59) Arabidopsis HAP2 (GCS1) is a sperm-specific gene required for pollen tube guidance and fertilization Development Epigenetic reprogramming in plant sexual reproduction Nat Rev Genet Epigenetic reprogramming and small RNA silencing of transposable elements in pollen Cell Emerging roles of linker histones in regulating chromatin structure and function Nat Rev Mol Cell Biol Transcriptomics analyses reveal the molecular roadmap and long non-coding RNA landscape of sperm cell lineage development Plant J The male germline of angiosperms: repertoire of an inconspicuous but important cell lineage Front Plant Sci The spatial association of the sperms cells and vegetative nucleus in the pollen grain of Brassica Protoplasma Linker histones are fine-scale chromatin architects modulating developmental decisions in Arabidopsis Genome Biol The evolution and functional divergence of the histone H2B family in plants PLoS Genet Chromatin remodelling during male gametophyte development Plant J Targeted reprogramming of H3K27me3 resets epigenetic memory in plant paternal chromatin Nat Cell Biol Induction of RNA-directed DNA methylation upon decondensation of constitutive heterochromatin EMBO Rep Natural depletion of histone H1 in sex cells causes DNA demethylation, heterochromatin decondensation and transposon activation eLife DNA methylation dynamics of sperm cell lineage development in tomato Plant J DNA demethylation by ROS1a in rice vegetative cells promotes methylation in sperm Proc Natl Acad Sci U S A Male gametophyte development in flowering plants: a story of quarantine and sacrifice JPlant Physiol The evolution and patterning of male gametophyte development Curr Top Dev Biol Transcriptomes of isolated Oryza sativa gametes characterized by deep sequencing: evidence for distinct sex-dependent chromatin and epigenetic states before fertilization Plant J Comparative transcriptomics of Arabidopsis sperm cells Plant Physiol Intercellular communication in Arabidopsis thaliana pollen discovered via AHG3 transcript movement from the vegetative cell to sperm Proc Natl Acad Sci U S A Clearance of maternal barriers by paternal miR159 to initiate endosperm nuclear division in Arabidopsis Nat Commun The nuclear envelope protein KAKU4 determines the migration order of the vegetative nucleus and sperm cells in pollen tubes JExp Bot Generative cell specification requires transcription factors evolutionarily conserved in land plants Curr Biol Building new insights in plant gametogenesis from an evolutionary perspective Nat Plants Small RNAs in pollen Sci China Life Sci Silencing in sperm cells is directed by RNA movement from the surrounding nurse cell Nat Plants RNA-directed DNA methylation PLoS Genet Sidecar pollen, an Arabidopsis thaliana male gametophytic mutant with aberrant cell divisions during pollen development Development The SIDECAR POLLEN gene encodes a microspore-specific LOB/AS2 domain protein required for the correct timing and orientation of asymmetric cell division Plant J Cited by (3) Integrated cytological and transcriptomic analysis reveals insights into pollen fertility in newly synthetic Brassica allohexaploids Epigenetic Dynamics and Regulation of Plant Male Reproduction Hormonal Signaling in the Progamic Phase of Fertilization in Plants Recommended articles (6) Graphene oxide and carbon nitride nanosheets co-modified silver chromate nanoparticles with enhanced visible-light photoactivity and anti-photocorrosion properties towards multiple refractory pollutants degradation Embryogenesis, endospermogenesis and fruit development in Lophophytum (Balanophoraceae): Focus on endosperm and embryo initiation NLRP3 inflammasome regulates Th17 differentiation in rheumatoid arthritis A Liquid Biopsy Assay for Noninvasive Identification of Lymph Node Metastases in T1 Colorectal Cancer A turbine disk-type triboelectric nanogenerator for wind energy harvesting and self-powered wildfire pre-warning Activation of transient receptor potential vanilloid channel 4 contributes to the development of ethanol-induced gastric injury in mice Videos

Current Opinion in Plant Biology

Volume 63,

October 2021

, 102118

Author links open overlay panel, ,

Abstract

Male germline development in flowering plants involves two distinct and successive phases, microsporogenesis and microgametogenesis, which involve one meiosis followed by two rounds of mitosis. Many aspects of distinctions after mitosis between the vegetative cell and the male germ cells are seen, from morphology to structure, and the differential functions of the two cell types in the male gametophyte are differentially needed and required for double fertilization. The two sperm cells, carriers of the hereditary substances, depend on the vegetative cell/pollen tube to be delivered to the female gametophyte for double fertilization. Thus, the intercellular communication and coordinated activity within the male gametophyte probably represent the most subtle regulation in flowering plants to guarantee the success of reproduction. This review will focus on what we have known about the differentiation process and the functional diversification of the vegetative cell and the male germ cell, the most crucial cell types for plant fertility and crop production.

Introduction

In flowering plants, a diploid pollen mother cell undergoes meiosis to produce a tetrad of haploid microspores, a process called microsporogenesis. Each microspore then undergoes microgametogenesis, a process which involves an asymmetric mitosis that generates two distinct cell types, one large vegetative cell (VC) and one small generative cell (GC), which continues one more round of mitosis to produce two sperm cells (SCs).

The production of haploid microspores in plant reproduction is comparable to how spermatids are formed by spermatocytes in animals. However, unlike in animals, an angiosperm male gametophyte contains more than one cell type. For example, in the model plant Arabidopsis, one male fertilization unit, termed the ‘male germ unit (MGU)’, contains two generative SCs and one somatic VC with the nucleus directly connected with the cytoplasmic projection of one SC [1].

Recent reviews discussed exciting advances in a few specific biological processes contributing to the formation and organization of the MGU, such as histone constitution [2, 3, 4], epigenetic modification [2,5•,6,7•,8,9,10••], distinct transcriptomes and proteomes [11, 12, 13, 14, 15, 16, 17, 18,19•,20•], and directional transport of small RNAs between the cells [21, 22, 23], and so on. In this review, we intend to highlight the critical regulators and mechanisms during early phases of the male germ line development, with emphasis on the processes of initial polarization and asymmetric mitosis of the microspore, as well as the specification of distinct daughter cell fates and function. We further discuss the model of ‘one-bus-two-passengers’ that describes the passive roles of the SCs during pollen tube delivery for double fertilization.

Section snippets

Asymmetric cell division of the microspores

Microspores are the spores of land plants that are formed from microspore mother cells inside the anther. The microspore undergoes an asymmetric cell division (ACD), pollen mitosis I (PMI), to differentiate two highly specialized cell types, the largeVCand the small GCthat undergoes another round of mitosis (pollen mitosis II, PMII) to produce two SCs. A typical mature male gametophyte (pollen) in the angiosperms is tricellular, containing one VC and two SCs. The VC constitutes the bulk of

Generative cell and vegetative cell: differing in the nucleus

Interestingly, after a microspore ACD, the adoption of a vegetative identity is probably the default pathway. This was evidently demonstrated by the phenotypes of a e2fa−/− fbl17±mutant in which uninucleated microspores with the VC identity are produced [33••]. In such a mutant, the cell-cycle transcription factor E2Fa together with its major downstream target FLB17 that inhibits the CDKA, 1 activity was mutated, resulting in the suppression of the G1/S–phase transition, thereby blocked PMI [

Physiological distinctions: sperm cells are passengers of the vegetative cell

Research in the past decades accumulated paramount of evidence supporting the predominant roles of the VC for the pollen tube to be guided and to deliver the SCs for double fertilization. In tobacco, ablation of the VC by cell-specific expression of DIPHTHERIA TOXIN Acauses the failure of the GC to migrate away from the pollen grain wall into the VC cytoplasm and ultimately the loss of viability [46]. In another study, a similar approach was used to damage the PMII. Interestingly, the

Conclusion

In nature, around 70% pollen development of flowering plants arrests in the bicellular stage [58]. The GC or SCs are engulfed in the larger VC with residue amount of cytoplasm. The expression profiles of the microspore shared more similarities with the somatic cells than its highly specialized daughter GC or SCs [14]. To some extent, the ACD of microspores is similar to stem cell differentiation, which produces daughter cells with distinct fate, intracellular elements, and physiology (Figure1

(Video) Reproduction in Flowering Plants - Formation of Male Gametophyte

Funding

Research in the L-JQ group is supported by the National Natural Science Foundation of China [Grant numbers 31991202, 31830004, and 31620103903] and that in JD group is supported by the National Institutes of Health (Grant number GM131827) and the National Science Foundation, United States (Grant numbers NSF 825885 and NSF 1952823). The scholarship from the China Scholarship Council (CSC) was awarded to J.H.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgement

The authors Thank to Qiupeng Lin from the Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, for help in making the figure.

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