Migration of sperm cells during pollen tube elongation in Arabidopsis thaliana: behavior during transport, maturation and upon dissociation of male germ unit associations

Ge, Li-Li; Gou, Xiaoping; Yuan, Tong; Strout, Greg; Nakashima, Jin; Blancaflor, Elison B.; Tian, Hui Qiao; Russell, Scott D.

doi:10.1007/s00425-010-1305-8

Cited by 23 publications

(16 citation statements)

References 24 publications

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“…Because the VN and the two SCs are connected, these two forces coordinate with each other to move the MGU forward. This double-driving force hypothesis is consistent with a reported observation that the SC projection that links the VN exhibited somewhat independent movement to the overall momentum of SCs (34). In addition, the bidirectional movement of the MGU was proposed to be a result of the dynamic balance between acropetal and basipetal forces (35).…”

Section: Discussionsupporting

confidence: 77%

Efficient plant male fertility depends on vegetative nuclear movement mediated by two families of plant outer nuclear membrane proteins

Zhou

Meier

2014

Proc. Natl. Acad. Sci. U.S.A.

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Increasing evidence suggests that nuclear migration is important for eukaryotic development. Although nuclear migration is conserved in plants, its importance for plant development has not yet been established. The most extraordinary plant nuclear migration events involve plant fertilization, which is starkly different from that of animals. Instead of evolving self-propelled sperm cells (SCs), plants use pollen tubes to deliver SCs, in which the pollen vegetative nucleus (VN) and the SCs migrate as a unit toward the ovules, a fundamental but barely understood process. Here, we report that WPP domain-interacting proteins (WIPs) and their binding partners the WPP domain-interacting tail-anchored proteins (WITs) are essential for pollen nuclear migration. Loss-offunction mutations in WIT and/or WIP gene families resulted in impaired VN movement, inefficient SC delivery, and defects in pollen tube reception. WIPs are Klarsicht/ANC-1/Syne-1 Homology (KASH) analogs in plants. KASH proteins are key players in animal nuclear migration. Thus, this study not only reveals an important nuclear migration mechanism in plant fertilization but also, suggests that similar nuclear migration machinery is conserved between plants and animals.nuclear envelope | Arabidopsis | male gametophyte | LINC complex N uclear migration is essential for cell differentiation, polarization, and migration, which influence organism development (1-3). Examples range from Caenorhabditis elegans P-cell development to mammalian neural development (1-3). The key players in opisthokont nuclear migration are the inner nuclear membrane Sad1/UNC-84 (SUN) proteins and outer nuclear membrane Klarsicht/ANC-1/Syne-1 Homology (KASH) proteins. SUN and KASH proteins form the linkers of the nucleoskeleton and the cytoskeleton complexes at the nuclear envelope (NE) and transfer cytoplasmic forces to the nucleus (1-3). In plants, nuclear migration is associated with a number of developmental events and environmental responses, including fertilization, root and leaf hair formation, and plant-microbe interactions (4, 5). So far, little is known about the mechanism of plant nuclear migration. Although SUN proteins are conserved in plants (6, 7), absence of animal KASH homologs in plants suggests that plants may have evolved different molecular solutions to achieve nuclear migration. Recently, WPP domaininteracting proteins (WIPs) were identified as KASH proteins in plants (8), and their outer nuclear membrane binding partners WPP domain-interacting tail anchored proteins (WITs) were shown to interact with myosin XI-I (9). The WIT-myosin XI

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Section: Discussionsupporting

confidence: 77%

Efficient plant male fertility depends on vegetative nuclear movement mediated by two families of plant outer nuclear membrane proteins

Zhou

Meier

2014

Proc. Natl. Acad. Sci. U.S.A.

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“…In fact, some sperm transcripts appear not to be translated into protein in sperm cells, but may display delayed expression (Bayer et al. , 2009), although others are clearly transcribed and translated inside sperm cells (Ge et al. , 2011).…”

Section: Discussionmentioning

confidence: 99%

Genomic profiling of rice sperm cell transcripts reveals conserved and distinct elements in the flowering plant male germ lineage

et al. 2012

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Summary Genomic assay of sperm cell RNA provides insight into functional control, modes of regulation, and contributions of male gametes to double fertilization. Sperm cells of rice (Oryza sativa) were isolated from field‐grown, disease‐free plants and RNA was processed for use with the full‐genome Affymetrix microarray. Comparison with Gene Expression Omnibus (GEO) reference arrays confirmed expressionally distinct gene profiles. A total of 10 732 distinct gene sequences were detected in sperm cells, of which 1668 were not expressed in pollen or seedlings. Pathways enriched in male germ cells included ubiquitin‐mediated pathways, pathways involved in chromatin modeling including histones, histone modification and nonhistone epigenetic modification, and pathways related to RNAi and gene silencing. Genome‐wide expression patterns in angiosperm sperm cells indicate common and divergent themes in the male germline that appear to be largely self‐regulating through highly up‐regulated chromatin modification pathways. A core of highly conserved genes appear common to all sperm cells, but evidence is still emerging that another class of genes have diverged in expression between monocots and dicots since their divergence. Sperm cell transcripts present at fusion may be transmitted through plasmogamy during double fertilization to effect immediate post‐fertilization expression of early embryo and (or) endosperm development.

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“…For the study of male and female germ units, the model plant Arabidopsis thaliana has been selected as the main experimental model. Studies on the segregation and function of male and female germ units have enriched theories of angiosperm reproductive biology (Ge et al, 2011;Huang and Russell, 1992). To elucidate the interactions between pollen and stigma, Ma et al (2013) comprehensively analyzed studies examining the characteristics of Corylus plants after selfcrossing or outcrossing pollination, focusing on the affinity between pollen and stigma.…”

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confidence: 99%

Pollen Tube Growth and Double Fertilization in Camellia oleifera

Gao¹,

Yuan²,

Yang³

et al. 2015

J. Amer. Soc. Hort. Sci.

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Camellia oleifera is an important plant species that produces edible oils. Understanding the double fertilization of this plant is critical for studies concerning crossbreeding, self-incompatibility, and the biological mechanisms underlying hybridization. We aimed to characterize pollen tube growth and double fertilization in C. oleifera. The female and male parent cultivars (Huashuo and Xianglin XLC15, respectively) were used for artificial pollination. Growth of the pollen tube in the style, ovary, and ovule from pollination to fertilization and the cytological characteristics of female and male gamete fusion during double fertilization were observed using fluorescence and scanning electron microscopy (SEM). Numerous pollen grains germinated 2 to 4 hours after pollination. The pollen tubes entered the interspaces between the papillar cells, grew along the stylar canal, and aggregated at the one-third site of the style. They grew in the gradually narrowing stylar canal, entering the locule. The tubes turned 90° and entered the embryo sac through the micropyle; subsequently, they entered a degenerated synergid, where the spermatids were released. One sperm nucleus fused with the polar nucleus, forming the primary endosperm nucleus, whereas the other sperm fused with the egg, forming the zygote. The polar nucleus was fertilized earlier than the egg. Double fertilization of C. oleifera is characterized as pre-mitotic gametogony. The current results lay a theoretical foundation for studies concerning the crossbreeding and embryology of C. oleifera and provide fundamental data concerning the reproductive biology of the genus Camellia.

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Migration of sperm cells during pollen tube elongation in Arabidopsis thaliana: behavior during transport, maturation and upon dissociation of male germ unit associations

Cited by 23 publications

References 24 publications

Efficient plant male fertility depends on vegetative nuclear movement mediated by two families of plant outer nuclear membrane proteins

Efficient plant male fertility depends on vegetative nuclear movement mediated by two families of plant outer nuclear membrane proteins

Genomic profiling of rice sperm cell transcripts reveals conserved and distinct elements in the flowering plant male germ lineage

Pollen Tube Growth and Double Fertilization in Camellia oleifera

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