Short Integuments1/suspensor1/carpel Factory, a Dicer Homolog, Is a Maternal Effect Gene Required for Embryo Development in Arabidopsis

Abstract

The importance of maternal cells in controlling early embryogenesis is well understood in animal development, yet in plants the precise role of maternal cells in embryogenesis is unclear. We demonstrated previously that maternal activity of the SIN1 (SHORT INTEGUMENTS1) gene of Arabidopsis is essential for embryo pattern formation and viability, and that its postembryonic activity is required for several processes in reproductive development, including flowering time control and ovule morphogenesis. Here, we report the cloning of SIN1, and demonstrate its identity to the CAF (CARPEL FACTORY) gene important for normal flower morphogenesis and to the SUS1 (SUSPENSOR1) gene essential for embryogenesis. SIN1/SUS1/CAF has sequence similarity to the Drosophila melanogaster gene Dicer, which encodes a multidomain ribonuclease specific for double-stranded RNA, first identified by its role in RNA silencing. The Dicer protein is essential for temporal control of development in animals, through the processing of small RNA hairpins that in turn inhibit the translation of target mRNAs. Structural modeling of the wild-type and sin1 mutant proteins indicates that the RNA helicase domain of SIN1/SUS1/CAF is important for function. The mRNA was detected in floral meristems, ovules, and early embryos, consistent with the mutant phenotypes. A 3.3-kb region 5Ј of the SIN1/SUS1/CAF gene shows asymmetric parent-of-origin activity in the embryo: It confers transcriptional activation of a reporter gene in early embryos only when transmitted through the maternal gamete. These results suggest that maternal SIN1/SUS1/CAF functions early in Arabidopsis development, presumably through posttranscriptional regulation of specific mRNA molecules.Molecular details behind genetic regulation in the early development of plants are beginning to emerge (for a recent review, see Chaudhury et al., 2001;Baroux et al., 2002). In Arabidopsis, only two genes have been identified whose activities are required in the maternal sporophyte (or female somatic cells) for normal pattern formation during embryo development (Ray et al., 1996b;Prigge and Wagner, 2000). Of these, SERRATE encodes a zinc finger protein presumably involved in chromatin structure modulation, and is required maternally for normal cotyledon initiation (Prigge and Wagner, 2000). At least one wild-type allele of SIN1 (SHORT INTEGUMENTS1), the only other gene identified in this class, is required in the maternal sporophyte for normal patterning in the embryo (Ray et al., 1996b). Plant strains homozygous for the hypomorphic sin1-2 mutant allele show a strong maternal effect on embryo development, producing developmentally arrested embryos with loss of apical, basal, or radial symmetry elements regardless of embryo genotype. Most of these form defective plants with no differentiation of shoot or root apical meristems (Ray et al., 1996b).The exact role of the mother plant in regulating embryogenesis is the subject of some debate. The discussion so far has focused on the role of gene products cont...

Endosperm: an integrator of seed growth and development

“…Direct maternal effects that originate from the central cell constitute an attractive hypothesis, but one that is supported by little, if any, direct evidence to date. The origin of the maternal effect of DICER-LIKE 1 remains mysterious [33], and the maternal effects that are associated with PROLIFERA (a homolog of MINICHRO-MOSOME MAINTENANCE 7) are complex and might involve several mechanisms [34].…”

Regulation of Ovule Development

“…By contrast, the integuments of dicer-like1 (dcl1, formerly short integuments1) mutants are shortened as a result of reduced cell elongation along the proximal-distal axis of the ovule ( Figure 6B) (Robinson-Beers et al, 1992;Ray et al, 1996a;Schauer et al, 2002). The DCL1 RNase III/RNA helicase is thought to be involved in the production or activity of small RNAs associated with the translational regulation of developmental genes (Jacobsen et al, 1999;Golden et al, 2002). Severe malformation of the inner and outer integuments results from mutations in TSO1 ( Figure 6C) .…”

The role of decapping proteins in the miRNA accumulation inArabidopsis thaliana

“…[18][19][20][21] dcl1-and ago1-null mutants show lethal phenotypes, indicating that miRNAs participate in plant development. [22][23][24][25] siRNAs originate from endogenous and exogenous doublestranded RNAs (dsRNAs). The dsRNAs are processed by DCL2, Decapping 1 (Dcp1), Decapping 2 (Dcp2) and VARIcOse (Vcs) are components of the decapping complex that removes the 7-methyl-guanosine 5'-diphosphate from the 5' end of mRNAs.…”