Arabidopsis haiku Mutants Reveal New Controls of Seed Size by Endosperm

Abstract

In flowering plants, maternal seed integument encloses the embryo and the endosperm, which are both derived from double fertilization. Although the development of these three components must be coordinated, we have limited knowledge of mechanisms involved in such coordination. The endosperm may play a central role in these mechanisms as epigenetic modifications of endosperm development, via imbalance of dosage between maternal and paternal genomes, affecting both the embryo and the integument. To identify targets of such epigenetic controls, we designed a genetic screen in Arabidopsis for mutants that phenocopy the effects of dosage imbalance in the endosperm. The two mutants haiku 1 and haiku 2 produce seed of reduced size that resemble seed with maternal excess in the maternal/paternal dosage. Homozygous haiku seed develop into plants indistinguishable from wild type. Each mutation is sporophytic recessive, and double-mutant analysis suggests that both mutations affect the same genetic pathway. The endosperm of haiku mutants shows a premature arrest of increase in size that causes precocious cellularization of the syncytial endosperm. Reduction of seed size in haiku results from coordinated reduction of endosperm size, embryo proliferation, and cell elongation of the maternally derived integument. We present further evidence for a control of integument development mediated by endosperm-derived signals.In flowering plants, the two female gametes, the egg cell and the central cell, are fertilized by one of the two male gametes delivered by the pollen tube. The zygotic product of the fusion of one male gamete with the egg cell develops into the embryo of the daughter plant. The fertilized central cell develops as the endosperm that nurtures embryo development. In most species, endosperm development is initiated by a proliferative syncytial phase accompanied by cell growth that generates a large multinucleate cell (Olsen, 2001; Berger, 2003). This syncytium is partitioned into individual cells by a specific type of cytokinesis called cellularization. In cereal species, the cellular endosperm stores the reserves of the seed during a phase marked by endoreduplication. Although the endosperm does not store the reserves of the seed in Arabidopsis, it most probably controls the flux of nutrients delivered by the vascular tissue of the mother to the embryo and protects the embryo from physical and osmotic stresses.Because the embryo is surrounded by the endosperm, which, in turn, is enclosed within the ovule integument, these three structures must coordinate their development to produce a mature seed of the appropriate size. The endosperm plays a central role in the control of seed size as indicated by a series of experiments in Arabidopsis and maize (Zea mays), where the dosage balance between maternal and paternal genomes was perturbed (Lin, 1984;Kermicle and Allemand, 1990;Scott et al., 1998). In most flowering plants, the endosperm contains two maternal copies and one paternal copy of the genome (2m/1p). In Arabidop...

The VQ Motif-Containing Protein Family of Plant-Specific Transcriptional Regulators

“…VQ14/HAIKU1 (IKU1) regulates the expression of MINISEED3 (MINI3; encoding a WRKY transcription factor) and IKU2 (encoding a Leu-rich repeat kinase), which are important for seed development (Garcia et al, 2003;Luo et al, 2005). The finding that the recessive vq14/iku1 mutant displays a smallseed phenotype indicates that VQ14 positively regulates endosperm growth and seed development.…”

Early Disruption of Maternal–Zygotic Interaction and Activation of Defense-Like Responses inArabidopsisInterspecific Crosses

“…Since the pollen-parent in our hybrid crosses was wild-type A. arenosa, only haploinsufficiency, additive, or maternal effects could be observed. Because of the effect of hybridity on maternal seed coat and genes involved in the flavonoid pathway, we included in the analysis the maternally expressed factor TRANS-PARENT TESTA GLABRA2 (TTG2) (Johnson et al, 2002;Garcia et al, 2005), which also affects interploidy hybrid lethality (Dilkes et al, 2008), and IKU2 because of its relationship to IKU1 and endosperm development (Garcia et al, 2003(Garcia et al, , 2005. The genetic backgrounds of these mutants, Col-0 and Landsberg erecta-0 (Ler-0), influence percentage of live seed.…”

Endosperm: an integrator of seed growth and development

“…No experimental data have yet been obtained for the role of the nucellus, but recent advances have demonstrated that interplay between endosperm and seed integument growth is essential for seed size determination in Arabidopsis (Figure 2). Mutations in the HAIKU (IKU) genes decrease endosperm size and eventually embryo and seed size [23]. The HAIKU genes IKU2 and MINISEED3 (MINI3) encode a leucine-rich-repeat kinase and a WRKY transcription factor, respectively [24].…”