An official website of the United States government
In angiosperms, double fertilization requires pollen tubes to transport non-motile sperm to distant egg cells housed in a specialized female structure known as the pistil, mediating the ultimate fusion between male and female gametes. During this journey, the pollen tube encounters numerous physical barriers that must be mechanically circumvented, including the penetration of the stigmatic papillae, style, transmitting tract, and synergid cells as well as the ultimate fusion of sperm cells to the egg or central cell. Additionally, the pollen tube must maintain structural integrity in these compact environments, while responding to positional guidance cues that lead the pollen tube to its destination. Here, we discuss the nature of these physical barriers as well as efforts to genetically and cellularly identify the factors that allow pollen tubes to successfully, specifically, and quickly circumnavigate them.
more »
« less
Synergid cell calcium oscillations refine understanding of FERONIA/LORELEI signaling during interspecific hybridization
Abstract Key messagePollen tubes from closely related species and mutants lacking pollen tube MYB transcription factors are able to initiate FER/LRE-dependent synergid cell calcium oscillations. AbstractReproductive isolation leads to the evolution of new species; however, the molecular mechanisms that maintain reproductive barriers between sympatric species are not well defined. In flowering plants, sperm cells are immotile and are delivered to female gametes by the pollen grain. After landing on the stigmatic surface, the pollen grain germinates a polarized extension, the pollen tube, into floral tissue. After growing via polar extension to the female gametes and shuttling its cargo of sperm cells through its cytoplasm, the pollen tube signals its arrival and identity to synergid cells that flank the egg. If signaling is successful, the pollen tube and receptive synergid cell burst, and sperm cells are released for fusion with female gametes. To better understand cell–cell recognition during reproduction and how reproductive barriers are maintained between closely related species, pollen tube-initiated synergid cell calcium ion dynamics were examined during interspecific crosses. It was observed that interspecific pollen tubes successfully trigger synergid cell calcium oscillations—a hallmark of reproductive success—but signaling fails downstream of key signaling genes and sperm are not released. This work further defines pollen tube–synergid cell signaling as a critical block to interspecific hybridization and suggests that the FERONIA/LORELEI signaling mechanism plays multiple parallel roles during pollen tube reception.
more »
« less
- Award ID(s):
- 1939255
- PAR ID:
- 10473133
- Publisher / Repository:
- Springer Science + Business Media
- Date Published:
- Journal Name:
- Plant Reproduction
- Volume:
- 37
- Issue:
- 1
- ISSN:
- 2194-7953
- Format(s):
- Medium: X Size: p. 57-68
- Size(s):
- p. 57-68
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Rising temperature extremes during critical reproductive periods threaten the yield of major grain and fruit crops. Flowering plant reproduction depends on the ability of pollen grains to generate a pollen tube, which elongates through the pistil to deliver sperm cells to female gametes for double fertilization. We used tomato as amodel fruit croptodeterminehowhigh temperature affects the pollen tube growthphase, takingadvantage of cultivars noted for fruit production in exceptionally hot growing seasons. We found that exposure to high temperature solely during the pollen tube growth phase limits fruit biomass and seed set more significantly in thermosensitive cultivars than in thermotolerant cultivars. Importantly, we found that pollen tubes from the thermotolerantTamaulipas cultivar have enhanced growth in vivo and in vitro under high temperature. Analysis of the pollen tube transcriptome’s response to high temperature allowed us to define two responsemodes (enhanced induction of stress responses and higher basal levels of growth pathways repressed by heat stress) associated with reproductive thermotolerance. Importantly, we define key components of the pollen tube stress response, identifyingenhancedreactive oxygenspecies (ROS)homeostasis andpollen tubecallose synthesis and deposition as important components of reproductive thermotolerance in Tamaulipas. Our work identifies the pollen tube growth phase as a viable target to enhance reproductive thermotolerance and delineates key pathways that are altered in crop varieties capable of fruiting under high-temperature conditions.more » « less
-
Abstract PremiseCo‐occurring plant species that share generalist pollinators often exchange pollen. This heterospecific pollen transfer (HPT) impacts male and female reproductive success through pollen loss and reductions in seed set, respectively. The resulting fitness cost of HPT imposes selection on reproductive traits (e.g., floral color and shape), yet we currently lack strong predictors for the post‐pollination fate of heterospecific pollen, especially within community and phylogenetic contexts. MethodsWe investigated the fate of heterospecific pollen at three distinct stages of plant reproduction: (1) pollen germination on the stigma, (2) pollen tube growth in the style, and (3) fertilization of ovules. We experimentally crossed 11 naturally co‐flowering species in the subalpine meadows of the Colorado Rocky Mountains, across a spectrum of phylogenetic relatedness. Using generalized linear mixed models and generalized linear models, we evaluated the effect of parental species identity and phylogenetic relatedness on pollen tube growth at each reproductive stage. ResultsWe found that heterospecific pollen tubes can germinate and grow within pistils at each reproductive stage, even when parental species are >100 My divergent. There was no significant effect of phylogenetic distance on heterospecific pollen success, and no evidence for a mechanism that suspends heterospecific pollen germination or pollen tube growth within heterospecific stigmas or styles. ConclusionsOur results show that even in communities where HPT is common, pre‐zygotic post‐pollination mechanisms do not provide strong barriers to interspecific fertilization. HPT can result in the loss of ovules even between highly diverged plant species.more » « less
-
Abstract Pollen tube attraction is a key event of sexual reproduction in flowering plants. In the ovule, two synergid cells neighboring the egg cell control pollen tube arrival via the active secretion of attractant peptides such as AtLURE1 and XIUQIU from the filiform apparatus (FA) facing toward the micropyle. Distinctive cell polarity together with longitudinal F-actin and microtubules are hallmarks of the synergid cell in various species, though the functions of these cellular structures are unclear. In this study, we used genetic and pharmacological approaches to indicate the roles of cytoskeletal components in FA formation and pollen tube guidance in Arabidopsis thaliana. Genetic inhibition of microtubule formation reduced invaginations of the plasma membrane but did not abolish micropylar AtLURE1.2 accumulation. By contrast, the expression of a dominant-negative form of ACTIN8 induced disorganization of the FA and loss of polar AtLURE1.2 distribution toward the FA. Interestingly, after pollen tube reception, F-actin became unclear for a few hours in the persistent synergid cell, which may be involved in pausing and resuming pollen tube attraction during early polytubey block. Our data suggest that F-actin plays a central role in maintaining cell polarity and in mediating male–female communication in the synergid cell.more » « less
-
The haploid female gametophyte (embryo sac) is an essential reproductive unit of flowering plants, usually comprising four specialized cell types, including the female gametes (egg cell and central cell). The differentiation of these cells relies on spatial signals which pattern the gametophyte along a proximal-distal axis, but the molecular and genetic mechanisms by which cell identities are determined in the embryo sac have long been a mystery. Recent identification of key genes for cell fate specification and their relationship to hormonal signaling pathways that act on positional cues has provided new insights into these processes. A model for differentiation can be devised with egg cell fate as a default state of the female gametophyte and with other cell types specified by the action of spatially regulated factors. Cell-to-cell communication within the gametophyte is also important for maintaining cell identity as well as facilitating fertilization of the female gametes by the male gametes (sperm cells).more » « less
