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The mathematics of sexual attraction.

Feijó JA - J. Biol. (2010)

Bottom Line: Pollen tubes follow attractants secreted by the ovules.In a recent paper in BMC Plant Biology, Stewman and colleagues have quantified the parameters of this attraction and used them to calibrate a mathematical model that reproduces the process and enables predictions on the nature of the female attractant and the mechanisms of the male response.

View Article: PubMed Central - HTML - PubMed

Affiliation: Instituto Gulbenkian de Ciência, P-2780-156 Oeiras, Portugal and Universidade de Lisboa, Faculdade de Ciências, Depto, Biologia Vegetal, Campo Grande C2, P-1749-016 Lisboa, Portugal. jfeijo@fc.ul.pt

ABSTRACT
Pollen tubes follow attractants secreted by the ovules. In a recent paper in BMC Plant Biology, Stewman and colleagues have quantified the parameters of this attraction and used them to calibrate a mathematical model that reproduces the process and enables predictions on the nature of the female attractant and the mechanisms of the male response.

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Ovule attraction and the chemotaxis of pollen tubegrowth. (a) Pollen tube guidance precedes double fertilization in flowering plants. A pollen tube carrying two sperm cells leaves the placenta to grow along the funiculus (the foot of the ovule) into the micropyle (the entrance of the ovule) following gradients generated by the maternal tissues of the ovule and by the female gametophyte. An embryo sac contains the egg apparatus (egg cell and two synergid cells), the central cell with two polar nuclei, and three antipodal cells. It is usually surrounded by a supportive tissue - the nucellus - and two layers of protective tissue - the inner and outer integuments. In Torenia the nucellus is disintegrated, generating a naked egg apparatus at the micropylar region. Adapted from [11]. (b, c) Semi-vivo growth system in Arabidopsis. Pollen is germinated in the stigma, but the style is cut (top in (b)) and co-cultivated with dissected ovules (bottom in (b)). When coming out of the style, pollen tubes grow in the surface of a semi-solid agar medium, and eventually target the micropyles of the ovules (c). If penetration is achieved, the contents of the tubes are discharged inside one synergid; if the system is carried out with pollen tubes (arrows in (c)) labeled with green fluorescent protein, the moment of fertilization is visible by fluorescence (arrowheads in (c)), and ovules can be scored in terms of successful attraction. The scale bars represent 100 mm. Adapted from [9]. (d) Depiction of the angles used in the analysis of pollen tube turning made by Stewman et al. [3]. These angles indicate how much the pollen tube would have to turn to take the most direct path toward the micropyle (qmp), and describe the new direction chosen by the pollen tube in response to the gradient (qtip). These quantitative data were then gathered for various incubation periods to deduce the nature and effect of the gradient produced by the diffusion of an attractant from the ovule's micropyle.
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Figure 2: Ovule attraction and the chemotaxis of pollen tubegrowth. (a) Pollen tube guidance precedes double fertilization in flowering plants. A pollen tube carrying two sperm cells leaves the placenta to grow along the funiculus (the foot of the ovule) into the micropyle (the entrance of the ovule) following gradients generated by the maternal tissues of the ovule and by the female gametophyte. An embryo sac contains the egg apparatus (egg cell and two synergid cells), the central cell with two polar nuclei, and three antipodal cells. It is usually surrounded by a supportive tissue - the nucellus - and two layers of protective tissue - the inner and outer integuments. In Torenia the nucellus is disintegrated, generating a naked egg apparatus at the micropylar region. Adapted from [11]. (b, c) Semi-vivo growth system in Arabidopsis. Pollen is germinated in the stigma, but the style is cut (top in (b)) and co-cultivated with dissected ovules (bottom in (b)). When coming out of the style, pollen tubes grow in the surface of a semi-solid agar medium, and eventually target the micropyles of the ovules (c). If penetration is achieved, the contents of the tubes are discharged inside one synergid; if the system is carried out with pollen tubes (arrows in (c)) labeled with green fluorescent protein, the moment of fertilization is visible by fluorescence (arrowheads in (c)), and ovules can be scored in terms of successful attraction. The scale bars represent 100 mm. Adapted from [9]. (d) Depiction of the angles used in the analysis of pollen tube turning made by Stewman et al. [3]. These angles indicate how much the pollen tube would have to turn to take the most direct path toward the micropyle (qmp), and describe the new direction chosen by the pollen tube in response to the gradient (qtip). These quantitative data were then gathered for various incubation periods to deduce the nature and effect of the gradient produced by the diffusion of an attractant from the ovule's micropyle.

Mentions: Curiously enough, answers to the question of the chemotaxis molecule's identity came from classical experimental embryology. For a long time, various teams have been developing partially artificial fertilization schemes, for either fundamental or applied reasons [6]. In most of these schemes, pollen is allowed to germinate in the stigma, but the style is excised and the pollen tubes are allowed to grow out of the style into an artificial medium. This semi-vivo method has more recently been combined with isolated ovules to test the hypothesis of whether the system is sufficient to provide attraction to the pollen tube; this would validate the existence of gradients of attractants secreted from the ovules. Such a system was first shown to work in the succulent plant Gasteria [8] and more recently in the model species Arabidopsis [9], the lily Lilium [10] and maize [11]. But none of these has been as powerful and informative as the system developed by Higashiyama and colleagues using the wishbone flower, Torenia fournieri [6]. Starting from the anatomical observation that in this species the female gametophyte - the embryo sac - is naked and exposed without any surrounding tissue, these authors [6] developed a series of experiments that showed for the first time the explosive discharge of the pollen tube inside the ovule and identified the synergid cells (Figure 2) as the source of the diffusing attractant signal [6]. In a tour-de-force of proteomics, the same authors recently isolated the first proteins to be shown to be specifically involved in the attractant signal: small, defensin-like, cysteine-rich peptides called LUREs [12]. A model of pollen tube attraction by diffusion of molecules from the micropyle now seems to be well established (Figure 2a). If comparisons can be drawn from the animal field [11], many more classes of proteins are expected to be described, as the proteomics effort is only just starting and many screening efforts are getting under way [7].


The mathematics of sexual attraction.

Feijó JA - J. Biol. (2010)

Ovule attraction and the chemotaxis of pollen tubegrowth. (a) Pollen tube guidance precedes double fertilization in flowering plants. A pollen tube carrying two sperm cells leaves the placenta to grow along the funiculus (the foot of the ovule) into the micropyle (the entrance of the ovule) following gradients generated by the maternal tissues of the ovule and by the female gametophyte. An embryo sac contains the egg apparatus (egg cell and two synergid cells), the central cell with two polar nuclei, and three antipodal cells. It is usually surrounded by a supportive tissue - the nucellus - and two layers of protective tissue - the inner and outer integuments. In Torenia the nucellus is disintegrated, generating a naked egg apparatus at the micropylar region. Adapted from [11]. (b, c) Semi-vivo growth system in Arabidopsis. Pollen is germinated in the stigma, but the style is cut (top in (b)) and co-cultivated with dissected ovules (bottom in (b)). When coming out of the style, pollen tubes grow in the surface of a semi-solid agar medium, and eventually target the micropyles of the ovules (c). If penetration is achieved, the contents of the tubes are discharged inside one synergid; if the system is carried out with pollen tubes (arrows in (c)) labeled with green fluorescent protein, the moment of fertilization is visible by fluorescence (arrowheads in (c)), and ovules can be scored in terms of successful attraction. The scale bars represent 100 mm. Adapted from [9]. (d) Depiction of the angles used in the analysis of pollen tube turning made by Stewman et al. [3]. These angles indicate how much the pollen tube would have to turn to take the most direct path toward the micropyle (qmp), and describe the new direction chosen by the pollen tube in response to the gradient (qtip). These quantitative data were then gathered for various incubation periods to deduce the nature and effect of the gradient produced by the diffusion of an attractant from the ovule's micropyle.
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Related In: Results  -  Collection

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Figure 2: Ovule attraction and the chemotaxis of pollen tubegrowth. (a) Pollen tube guidance precedes double fertilization in flowering plants. A pollen tube carrying two sperm cells leaves the placenta to grow along the funiculus (the foot of the ovule) into the micropyle (the entrance of the ovule) following gradients generated by the maternal tissues of the ovule and by the female gametophyte. An embryo sac contains the egg apparatus (egg cell and two synergid cells), the central cell with two polar nuclei, and three antipodal cells. It is usually surrounded by a supportive tissue - the nucellus - and two layers of protective tissue - the inner and outer integuments. In Torenia the nucellus is disintegrated, generating a naked egg apparatus at the micropylar region. Adapted from [11]. (b, c) Semi-vivo growth system in Arabidopsis. Pollen is germinated in the stigma, but the style is cut (top in (b)) and co-cultivated with dissected ovules (bottom in (b)). When coming out of the style, pollen tubes grow in the surface of a semi-solid agar medium, and eventually target the micropyles of the ovules (c). If penetration is achieved, the contents of the tubes are discharged inside one synergid; if the system is carried out with pollen tubes (arrows in (c)) labeled with green fluorescent protein, the moment of fertilization is visible by fluorescence (arrowheads in (c)), and ovules can be scored in terms of successful attraction. The scale bars represent 100 mm. Adapted from [9]. (d) Depiction of the angles used in the analysis of pollen tube turning made by Stewman et al. [3]. These angles indicate how much the pollen tube would have to turn to take the most direct path toward the micropyle (qmp), and describe the new direction chosen by the pollen tube in response to the gradient (qtip). These quantitative data were then gathered for various incubation periods to deduce the nature and effect of the gradient produced by the diffusion of an attractant from the ovule's micropyle.
Mentions: Curiously enough, answers to the question of the chemotaxis molecule's identity came from classical experimental embryology. For a long time, various teams have been developing partially artificial fertilization schemes, for either fundamental or applied reasons [6]. In most of these schemes, pollen is allowed to germinate in the stigma, but the style is excised and the pollen tubes are allowed to grow out of the style into an artificial medium. This semi-vivo method has more recently been combined with isolated ovules to test the hypothesis of whether the system is sufficient to provide attraction to the pollen tube; this would validate the existence of gradients of attractants secreted from the ovules. Such a system was first shown to work in the succulent plant Gasteria [8] and more recently in the model species Arabidopsis [9], the lily Lilium [10] and maize [11]. But none of these has been as powerful and informative as the system developed by Higashiyama and colleagues using the wishbone flower, Torenia fournieri [6]. Starting from the anatomical observation that in this species the female gametophyte - the embryo sac - is naked and exposed without any surrounding tissue, these authors [6] developed a series of experiments that showed for the first time the explosive discharge of the pollen tube inside the ovule and identified the synergid cells (Figure 2) as the source of the diffusing attractant signal [6]. In a tour-de-force of proteomics, the same authors recently isolated the first proteins to be shown to be specifically involved in the attractant signal: small, defensin-like, cysteine-rich peptides called LUREs [12]. A model of pollen tube attraction by diffusion of molecules from the micropyle now seems to be well established (Figure 2a). If comparisons can be drawn from the animal field [11], many more classes of proteins are expected to be described, as the proteomics effort is only just starting and many screening efforts are getting under way [7].

Bottom Line: Pollen tubes follow attractants secreted by the ovules.In a recent paper in BMC Plant Biology, Stewman and colleagues have quantified the parameters of this attraction and used them to calibrate a mathematical model that reproduces the process and enables predictions on the nature of the female attractant and the mechanisms of the male response.

View Article: PubMed Central - HTML - PubMed

Affiliation: Instituto Gulbenkian de Ciência, P-2780-156 Oeiras, Portugal and Universidade de Lisboa, Faculdade de Ciências, Depto, Biologia Vegetal, Campo Grande C2, P-1749-016 Lisboa, Portugal. jfeijo@fc.ul.pt

ABSTRACT
Pollen tubes follow attractants secreted by the ovules. In a recent paper in BMC Plant Biology, Stewman and colleagues have quantified the parameters of this attraction and used them to calibrate a mathematical model that reproduces the process and enables predictions on the nature of the female attractant and the mechanisms of the male response.

Show MeSH
Related in: MedlinePlus