Maternal Gametophyte Effects on Seed Development in Maize

Abstract

Flowering plants, like placental mammals, have an extensive maternal contribution toward progeny development. Plants are distinguished from animals by a genetically active haploid phase of growth and development between meiosis and fertilization, called the gametophyte. Flowering plants are further distinguished by the process of double fertilization that produces sister progeny, the endosperm and the embryo, of the seed. Because of this, there is substantial gene expression in the female gametophyte that contributes to the regulation of growth and development of the seed. A primary function of the endosperm is to provide growth support to its sister embryo. Several mutations in Zea mays subsp. mays have been identified that affect the contribution of the mother gametophyte to the seed. The majority affect both the endosperm and the embryo, although some embryo-specific effects have been observed. Many alter the pattern of expression of a marker for the basal endosperm transfer layer, a tissue that transports nutrients from the mother plant to the developing seed. Many of them cause abnormal development of the female gametophyte prior to fertilization, revealing potential cellular mechanisms of maternal control of seed development. These effects include reduced central cell size, abnormal architecture of the central cell, abnormal numbers and morphology of the antipodal cells, and abnormal egg cell morphology. These mutants provide insight into the logic of seed development, including necessary features of the gametes and supporting cells prior to fertilization, and set up future studies on the mechanisms regulating maternal contributions to the seed.

Keywords: embryo sac; endosperm transfer layer; gametophyte; maize; maternal effect.

Figure 1

Ears of maternal-effect mutants. (A) Wild-type W22 female pollinated by +/ssc1; enr1-m with all normal kernels, showing the strict maternal effect. (B–Q) Maternal-effect mutant heterozygous females crossed by wild-type pollen. (B) +/ssc1; enr1-m W22 female by wild-type male. Germless mutant kernels with intense pigmentation of R1-r::(Venezuela). (C) +/Mn-Uq W22. (D) +/tpn1 Mo17. (E) +/bsl2 B104. (F) +/nol1 B104. (G) +/hrl1 B104. (H) +/hrl2 W22. (I) +/sba1 W22. (J) +/mrn1 B73. (K) +/mrn2 W22. (L) +/mrn3 W22. (M) +/nbe1 W22. (N) +/stt2 B73. (O) +/stt3 Mo17, note the linkage between the small kernel phenotype and R1-r::standard (purple/brown kernels). (P) +/ecr1 W22. (Q) +/ecr2 W22. Arrowheads indicate representative defective kernels on each ear. Ear tips and hence the germinal sides of the kernels are all to the left. Bar, 1.0 cm. WT, wild type.

Figure 2

Map position of maternal-effect mutants. The 10 chromosomes of maize are shown. Boundaries between chromosome bins are shown with horizontal white lines. Centromeres are marked by constrictions. Approximate map positions of maternal-effect mutants (including previously published mutants) are shown. See Table S1 for supporting data.

Figure 3

Mature kernels of maternal-effect mutants. Germinal (embryo) face (left) and a median longitudinal section (right) through the center of the embryo (or where the embryo would be). Mutant kernels are from heterozygous mutant females crossed by wild-type pollen. The embryo in the longitudinal section is oriented to the left in all kernels. (A) Wild type, (B) ssc1, (C) Mn-Uq, (D) tpn1, (E) bsl2, (F) nol1, (G) hrl1, (H) hrl2, (I) sba1, (J) mrn1, (K) mrn2, (L) mrn3, (M) nbe1, (N) stt2, (O) stt3, (P) ecr1, and (Q) ecr2. e, embryo; f, floury endosperm; v, vitreous endosperm. All kernels are shown at the same scale. Bar, 0.5 cm.

Figure 4

Mature embryo-sac phenotypes in plants heterozygous of maternal-effect mutants. The micropylar end is at the bottom and the chalazal end at the top of each panel. The future germinal side of the kernel is oriented toward the right of each panel. (A and Q) Wild type. (B) ssc1. (C) bsl2 with polar nuclei against the future germinal side. (D) nol1 with polar nuclei against the future germinal side. (E) hrl1 in W64A with few normal sized antipodal cells. (F) hrl1 in Mo17 with few, large antipodal cells. (G) sba1 with polar nuclei against the future abgerminal side and few antipodal cells. (H) mrn1 with polar nuclei near the chalazal end of the central cell and with few antipodal cells. (I) mrn1 with polar nuclei against the future germinal side. (J) mrn2 with extra cells near the antipodal cell cluster. (K) mrn2 embryo sac arrested at 2-nucleate stage. (L) mrn3 embryo sac arrested at the 2-nucleate stage. (M) stt2 small embryo sac with few antipodal cells like stt1. (N) stt3 small embryo sac with few antipodal cells like stt1. (O) stt3 with duplicated embryo sac. (P) ecr1 small embryo sac with small egg cell. (Q) Close up of wild-type egg cell. Note enlarged egg cell with centrally positioned nucleus surrounded by cytoplasmic strands. The brightly fluorescent material next to the egg cell is the remnant of a synergid. (R) Close up of egg found in ssc1. The egg cell has expanded, but all cytoplasmic contents are at the micropylar end like an immature synergid. (S) Close up of small egg cell in ecr1. (A–P) Bar, 100 µm. (Q–S) Bar, 20 µm. a, antipodal cell cluster; a*, abnormal antipodal cell cluster; cc, central cell; e, egg cell; pn, polar nuclei; WT, wild type; xc, extra cells.

Figure 5

Pattern of expression of pBET1::GUS in maternal-effect mutants. (A) Wild type 20 DAP, (B) wild type 35 DAP, (C) ssc1, (D) Mn-Uq, (E) tpn1, (F) bsl2, (G) nol1, (H) hrl1, (I) hrl2, (J) sba1, (K) mrn1, (L) mrn2, (M) mrn3, (N) nbe1, (O) stt2, (P) stt3, (Q) ecr1, and (R) ecr2. (B–F and H–R) Kernels are between 33 and 37 DAP. (A and G) Kernels are 20 DAP. Kernels are shown at the same scale. Bar, 0.5 cm. WT, wild type.