Mechanistic insights from a quantitative analysis of pollen tube guidance

Abstract

BackgroundPlant biologists have long speculated about the mechanisms that guide pollen tubes to ovules. Although there is now evidence that ovules emit a diffusible attractant, little is known about how this attractant mediates interactions between the pollen tube and the ovules.ResultsWe employ a semi-in vitro assay, in which ovules dissected from Arabidopsis thaliana are arranged around a cut style on artificial medium, to elucidate how ovules release the attractant and how pollen tubes respond to it. Analysis of microscopy images of the semi-in vitro system shows that pollen tubes are more attracted to ovules that are incubated on the medium for longer times before pollen tubes emerge from the cut style. The responses of tubes are consistent with their sensing a gradient of an attractant at 100-150 μm, farther than previously reported. Our microscopy images also show that pollen tubes slow their growth near the micropyles of functional ovules with a spatial range that depends on ovule incubation time.ConclusionsWe propose a stochastic model that captures these dynamics. In the model, a pollen tube senses a difference in the fraction of receptors bound to an attractant and changes its direction of growth in response; the attractant is continuously released from ovules and spreads isotropically on the medium. The model suggests that the observed slowing greatly enhances the ability of pollen tubes to successfully target ovules. The relation of the results to guidance in vivo is discussed.

Two Mitogen-Activated Protein Kinases, MPK3 and MPK6, Are Required for Funicular Guidance of Pollen Tubes in Arabidopsis

“…To examine if mpk3 mpk6 pollen is also defective in micropylar guidance, we performed a semi-in vitro pollen tube guidance assay, which recapitulates pollen tube navigation by micropylar attractants (Palanivelu and Preuss, 2006;Stewman et al, 2010), using pollen from mpk3 -/-mpk6 -/-gMPK6-YFP +/-TdTOM +/+ plants. The results showed that double mutant pollen tubes were not defective in navigation to the micropyle (ovules targeted by mpk3 mpk6 TdTOM:mpk3 mpk6 gMPK6-YFP TdTOM pollen = 43:46, expected 1:1, P = 0.75).…”

The mathematics of sexual attraction

“…However, the evidence seems to implicate many other non-specific, small, diffusible chemicals, such as ions or even the signaling gas nitric oxide (NO) [10]. In fact, the involvement of NO is not a surprise, because various behaviors shown by pollen tubes when NO concentration is disturbed seem to indicate a slowing down of growth of the pollen tube as it approaches the diffusion source; these effects fit with those found in the model of Stewman and colleagues [3]. …”

“…Stewman et al [3] have now carefully analyzed the growth curvature angles of Torenia pollen tubes (Figure 2d) in various experimental conditions, namely with different incubation times of the ovules (presumably corresponding to different levels of a standing gradient), and could thus determine important quantitative parameters of the attraction process. First, they found that the gradient action could extend a distance of 100 to 150 mm [3], a distance significantly longer than had been previously thought [6,9] or than had been experimentally tested with artificial gradients of isolated molecules [2,12]. This distance estimate probably means that various types of molecules with different ranges and actions come together to produce the biological reaction.…”

“…Mathematics is now being used to investigate the problem for the first time, in a ground-breaking article recently published in BMC Plant Biology [3]. In this study, Stewman and colleagues use a semi-vivo system to better quantify the nature and range of the ovule's attractants.…”

Developing a Global Perspective in / FOR Science Teacher Education: The Case of Pollination

“…Finally, I conclude the class by talking about different ways the same ideas could be reproduced in different classroom environments -like the production of public announcement radio podcasts, development of fundraising activities, fieldtrips to the outdoors, and the creation of environmental ad campaigns. In part due to our "plant blindness" (Manetas, 2012;Wandersee & Schussler, 1999), pollination goes unnoticed even though it is complexly beautiful (Pollan, 2001;Stewman et al, 2010). Consequently, the "regulating services" provided 497 by pollinators (i.e., pest and disease control) and the "supporting services" delivered through the occurrence of pollination itself (i.e., crop pollination) (Millennium Ecosystem Assessment, 2005) can be simply too easily neglected in science (teacher) education.…”