Kin recognition within a seed and the effect of genetic relatedness of an endosperm to its compatriot embryo on maize seed development

Abstract

As one of two sexual products resulting from double fertilization in angiosperms, the endosperm nourishes its compatriot embryo during seed development and/or germination and ultimately dies. Theoretical studies suggest that the genetic relatedness of an endosperm to its embryo in the same seed might determine the amount of resources ultimately available for the embryo during seed development. We took advantage of the phenomenon of heterofertilization in cultivated maize to empirically test whether genetic relatedness between a triploid embryo-nourishing endosperm and its compatriot diploid embryo impacts the process of resource allocation between these two sexually produced entities. We used genetically distinct maize inbred lines to perform two crossing experiments. Dry weights of dissected embryos and endosperms of mature heterofertilized and adjacent homofertilized kernels were compared. Embryo weight of heterofertilized kernels was significantly less than that of embryos of homofertilized kernels, whereas there was no significant difference in endosperm weight between the two types of kernels. Our results suggest that the degree of genetic relatedness of an endosperm to its compatriot embryo affects seed development and specifically the amount of maternal resources allocated to an endosperm that are eventually turned over to an embryo. The lower the coefficient of relatedness of an endosperm to its compatriot embryo, the smaller the embryo. Thus, the endosperm of a heterofertilized seed appears to behave less cooperatively with respect to resource transfer toward its less closely related embryo compared with the endosperm of a homofertilized seed.

Fig. 1.

Coefficients of relatedness and hypothetical patterns of resource allocation in homofertilized and heterofertilized maize kernels. (A) Heterofertilization does not alter the relationship between the maternal sporophyte and the endosperm, but decreases the coefficient of relatedness of an endosperm to its compatriot embryo, r_(En˗CEm), relative to homofertilization. If r_(En˗CEm) predicts allocation, then the size of the endosperm should not differ, but embryos should be smaller in heterofertilized kernels. (B) Heterofertilization decreases the relatedness ratio, r_(En˗CEm)/r_(En˗OEm), a theoretical indicator of the aggressiveness with which an endosperm will garner resources from the maternal sporophyte. The relatedness ratio predicts that heterofertilized endosperms and kernels should be smaller than those resulting from homofertilization. Numbers in parentheses above the arrows indicate the coefficient of relatedness of one entity to the other when the parents are highly homozygous and unrelated (Table S1). Solid arrows indicate resource transfer, and the thickness indicates relative amount of transfer. Dashed arrows indicate the coefficient of relatedness of an endosperm to an embryo in another kernel. Color of endosperm or embryo indicates the source of the paternal genome. MS indicates maternal sporophyte.

Fig. 2.

Homofertilized and heterofertilized kernels from cross A (upper four panels) and cross B (lower four panels). B73 is the maternal sporophyte for all crosses. The paternal genetic background and the state of R1 locus in endosperms and embryos are indicated for each possible outcome of mixed pollinations. YY, yellow endosperm with yellow embryo; PP, purple endosperm with purple embryo; YP, yellow endosperm with purple embryo; PY, purple endosperm with yellow embryo.