The endosperm-specificZHOUPIgene ofArabidopsis thalianaregulates endosperm breakdown and embryonic epidermal development

Abstract

During Arabidopsis seed development, the growing embryo invades and consumes the surrounding endosperm tissue. The signalling pathways that coordinate the separation of the embryo from the endosperm and the concomitant breakdown of the endosperm are poorly understood. We have identified a novel bHLH transcription factor, ZHOUPI (ZOU), which mediates these processes. ZOU is expressed exclusively in the endosperm of developing seeds. It is activated in the central cell immediately after fertilization and is initially expressed uniformly in endosperm, subsequently resolving to the embryo surrounding region (ESR). However, zou mutant embryos have defects in cuticle formation and in epidermal cell adhesion, suggesting that ZOU functions non-autonomously to regulate embryonic development. In addition, the endosperm of zou mutant seeds fails to separate from the embryo, restricting embryo expansion and resulting in the production of shrivelled collapsed seeds. zou seeds retain more endosperm than do wild-type seeds at maturity, suggesting that ZOU also controls endosperm breakdown. We identify several target genes whose expression in the ESR is regulated by ZOU. These include ABNORMAL LEAF SHAPE1, which encodes a subtilisinlike protease previously shown to have a similar role to ZOU in regulating endosperm adhesion and embryonic epidermal development. However, expression of several other ESR-specific genes is independent of ZOU. Therefore, ZOU is not a general regulator of endosperm patterning, but rather controls specific signalling pathways that coordinate embryo invasion and breakdown of surrounding endosperm tissues.

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

“…ZHOUPI encodes a basic helixloop-helix endosperm transcription factor that regulates development of the embryo-endosperm interface through targets, including ALE1. Loss of either ALE1 or ZHOUPI results in shriveled seed whose embryos lack a proper cuticle (Yang et al, 2008). ALE1 expression was significantly reduced in Col-0 hybrids, but not in C24 hybrids, consistent with ZHOUPI regulation.…”

“…FIS2, HAIKU1, SEEDSTICK/ AGL11, SHORT ROOT, HOMEODOMAIN GLABROUS9 (HDG9), HDG10, and ZHOUPI/RETARDED GROWTH OF EMBRYO1 (Chaudhury et al, 1997;Luo et al, 2000;Kondou et al, 2008;Yang et al, 2008;Mizzotti et al, 2012) were all misregulated in comparison to control crosses. A subset of these genes, FIS2, HDG9, and HDG10, is coexpressed during development ( Figure 2; see Supplemental Figure 8A online).…”

The Time Required for Dormancy Release in Arabidopsis Is Determined by DELAY OF GERMINATION1 Protein Levels in Freshly Harvested Seeds

“…These were the endosperm-specific promoters Pro At-FIS2, Pro At-ZHOUPI, and Pro Nt-CAT1 (Suzuki et al, 1995;Luo et al, 2000;Yang et al, 2008), the epidermal layer of the embryo-specific promoter Pro At-ML1 (Sessions et al, 1999), the meristem-specific promoters Pro At-STM and Pro At-CLV3 (Long et al, 1996), and the phloem-specific promoter Pro At-SUC2 (Juergensen et al, 2003). At-STM, At-ML1, and At-SUC2 promoter entry clones were a gift from George Coupland , and CAT1 promoter was a gift from Gerhard Leubner (Leubner-Metzger, 2005).…”

Genomic Imprinting Was Evolutionarily Conserved during Wheat Polyploidization

“…The resulting endosperm, a functional analog of the placenta in mammals, facilitates embryogenesis and supports seedling growth by providing the embryo with nutrients. The endosperm tissue also interacts dynamically with the embryo over the course of development by activating important signaling pathways that are required for embryo development (Yang et al, 2008;Fouquet et al, 2011;Costa et al, 2014;Xu et al, 2014). Therefore, proper endosperm development is essential for coordinating embryo and seed growth.…”