Ploidy and the evolution of endosperm of flowering plants

Abstract

In angiosperms, spermatozoa go by pair in each pollen grain and fertilize, in addition to the egg cell, one of its sister cells, called the central cell. This "double fertilization" leads to the embryo on the one hand and to its nutritive tissue, the endosperm, on the other hand. In addition, in most flowering plants, the endosperm is triploid because of a doubled maternal genetic contribution in the central cell. Most of the hypotheses trying to explain these eccentricities rest on the assumption of a male/female conflict over seed resource allocation. We investigate an alternative hypothesis on the basis of the masking of deleterious alleles. Using analytical methods, we show that a doubled maternal contribution and double fertilization tend to be favored in a wide range of conditions when deleterious mutations alter the function of the endosperm. Furthermore, we show that these conditions vary depending on whether these traits are under male or female control, which allows us to describe a new type of male/female conflict.

Figure 1.—

Timing of resource accumulation in the seed. All the resources are allocated before fertilization in cycads and ginkgoes. Resources are allocated both before and after fertilization in conifers and all the resources are allocated after fertilization in angiosperms.

Figure 2.—

Possible scenarios for the evolution of the genetic makeup of the embryo nutritive tissue, modified from Friedman and Ryerson (2009). In the left scenario, there are one 1m:0p → 1m:1p transition and two 1m:1p → 2m:1p transitions and thus three steps. In the right scenario, there are one 1m:0p → 2m:0p transition, one 2m:0p → 2m:1p transition, and two 2m:1p → 1m:1p transitions and thus four steps. In addition, the latter scenario involves a 2m:0p state that has never been observed in any taxa.

Figure 3.—

Life cycle. The sporophyte is born from the fertilization of a male gamete and a female gamete. These gametes are produced by the male and female gametophytes (the pollen and the embryo sac, respectively). In the sporophyte's sexual organs, meiosis produces spores that develop in new gametophytes.

Figure 4.—

Illustration of the QLE analysis of the DF and MCD models. The direction of selection at the modifier locus is indicated for different h (x-axis) and R (y-axis) values. In A and B (DF model), 1m:1p is favored in the shaded area whereas 1m:0p is favored in the open area. In C and D (MCD model), 2m:1p is favored in the shaded area whereas 1m:1p is favored in the open area. A, C and B, D illustrate paternal and maternal expression of the modifier locus, respectively. In all panels, the dashed area corresponds to a negative linkage disequilibrium (the modifier is associated to the purged chromosome). Direct selection favors DF on the left-hand side of the dashed line (which is , A and B), whereas it favors MCD on the right-hand side of the dashed line (which is h = h_m = 0.3, C and D). The QLE approximation becomes inaccurate when R is very low (the points represent critical h values obtained directly from exact simulations). Parameter values are s = 5 × 10⁻², μ = 10⁻³, υ = 0.1, δ_υ = 0.01, h₁ = 0.2, and h₂ = 0.4.

Figure 5.—

Illustration of the stability analysis of DF and MCD models. The direction of selection at the modifier locus is indicated for different dominance (h, x-axis) and recombination values (R, y-axis). In A and B (DF model), 1m:1p is favored in the area with dark shading [that corresponds to the pairwise invasibility plot (PIP) a], whereas 1m:0p is favored in the open area (that corresponds to PIP e). The areas with intermediate shading correspond to b, c, and d, that is, to cases where (b) DF is only convergent stable, (c) an intermediary, unstable equilibrium exists, and (d) DF is not convergent stable. In C and D (MCD model), 2m:1p is favored in the shaded area whereas 1m:1p is favored in the open area. We can see that the intermediate cases are indistinguishable for the MCD model. The parameters values are h₁ = 0.2, h₂ = 0.4, μ = 10⁻³, and s = 10⁻¹.

Figure 6.—

Combined evolution of DF and MCD. The different possible scenarios for the combined evolution of DF and MCD are shown when . (h₁ = 0.6 and h₂ = 0.2 in this example, yielding h_m = 0.4). The solid lines indicate the critical maternal and paternal h values for DF model. The dashed lines indicate the critical maternal and paternal h values for MCD model. In area 1, DF is favored, and MCD is not (1m:1p is thus expected to evolve). In area 2, both DF and MCD are favored (2m:1p evolves). In area 3, DF is favored and MCD is favored only if under maternal control (thus either 1m:1p or 2m:1p may evolve depending on which sex predominantly controls MCD). In area 4, DF is favored only if under paternal control, and MCD is not favored (thus either 1m:0p or 1m:1p may evolve). In area 5 DF is favored only if under paternal control, while MCD is favored only if under maternal control, and thus 1m:0p, 1m:1p, or 2m:1p may be favored. In area 6 DF is favored only if under paternal control and MCD is always favored (either 1m:1p or 2m:1p may evolve). Eventually, in area 7 neither DF nor MCD is favored, and 1m:0p evolves. The figure is drawn using the results of the stability analysis and with μ = 10⁻³, s = 10⁻¹, ν_M = 0.1, and ν_m = 0.1.

Figure 7.—

Comparison of the conditions for the evolution of diploidy and DF. The overlap of the conditions of h and R is shown, where diploidy (2N) is favored by the conditions of h and R where DF is favored. Indeed, 2N is favored on the left of the dashed line, while DF is favored on the left of the solid lines (the left solid line corresponds to the case of a maternal expression of the modifier locus and the right solid line corresponds to the case of a paternal expression of the modifier locus). The figure is drawn using the results of the stability analysis and with s = 10⁻¹, μ = 10⁻³, ν_M = 0.1, and ν_m = 0.1.