Transcriptome Analysis of Proliferating Arabidopsis Endosperm Reveals Biological Implications for the Control of Syncytial Division, Cytokinin Signaling, and Gene Expression Regulation

Day, Robert C.; Herridge, Rowan P.; Ambrose, Barbara A.; Macknight, Richard C.

doi:10.1104/pp.108.128108

Cited by 138 publications

(125 citation statements)

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“…The high level of cytokinin activity found in endosperm suggested that the plant hormone cytokinin regulates growth of seed components and controls seed mass or yield (53)(54)(55). More specifically, syncytial endosperm produces high amounts of cytokinin in many plant species such as coconut, maize, and rice (36,54,56,57).…”

Section: Discussionmentioning

confidence: 99%

Integration of epigenetic and genetic controls of seed size by cytokinin in Arabidopsis

Nie

Tan

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

105

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The development of seeds in flowering plants is placed under complex interactions between maternal tissues, the embryo, and the endosperm. The endosperm plays a major role in the regulation of seed size. In Arabidopsis thaliana, endosperm size depends on the coordination of the genetic pathway HAIKU (IKU) with epigenetic controls comprising genome dosage, DNA methylation, and trimethylated lysine 27 on histone H3 (H3K27me3) deposition. However, the effectors that integrate these pathways have remained unknown. Here, we identify a target of the IKU pathway, the cytokinin oxidase CKX2, that affects cytokinin signaling. CKX2 expression is activated by the IKU transcription factor WRKY10 directly and promotes endosperm growth. CKX2 expression also depends on H3K27me3 deposition, which fluctuates in response to maternal genome dosage imbalance and DNA demethylation of male gametes. Hence, the control of endosperm growth by CKX2 integrates genetic and epigenetic regulations. In angiosperms, cytokinins are highly active in endosperm, and we propose that IKU effectors coordinate environmental and physiological factors, resulting in modulation of seed size.

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Section: Discussionmentioning

confidence: 99%

Integration of epigenetic and genetic controls of seed size by cytokinin in Arabidopsis

Nie

Tan

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

105

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“…Only a few of these studies, however, have focused exclusively on seeds and/or embryos to identify important regulators and processes required for seed development (27)(28)(29)(30)(31). In this paper, we present results of Affymetrix GeneChip experiments that profile genes that are active before, during, and after Arabidopsis seed formation.…”

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confidence: 99%

Global analysis of gene activity duringArabidopsisseed development and identification of seed-specific transcription factors

Le¹,

Cheng²,

Bui³

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

514

493

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Most of the transcription factors (TFs) responsible for controlling seed development are not yet known. To identify TF genes expressed at specific stages of seed development, including those unique to seeds, we used Affymetrix GeneChips to profile Arabidopsis genes active in seeds from fertilization through maturation and at other times of the plant life cycle. Seed gene sets were compared with those expressed in prefertilization ovules, germinating seedlings, and leaves, roots, stems, and floral buds of the mature plant. Most genes active in seeds are shared by all stages of seed development, although significant quantitative changes in gene activity occur. Each stage of seed development has a small gene set that is either specific at the level of the GeneChip or up-regulated with respect to genes active at other stages, including those that encode TFs. We identified 289 seed-specific genes, including 48 that encode TFs. Seven of the seed-specific TF genes are known regulators of seed development and include the LEAFY COTYLEDON ( LEC ) genes LEC1, LEC1-LIKE, LEC2 , and FUS3 . The rest represent different classes of TFs with unknown roles in seed development. Promoter-β -glucuronidase ( GUS ) fusion experiments and seed mRNA localization GeneChip datasets showed that the seed-specific TF genes are active in different compartments and tissues of the seed at unique times of development. Collectively, these seed-specific TF genes should facilitate the identification of regulatory networks that are important for programming seed development.

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“…A first difficulty encountered in the characterization of MADS box type I members was their very low expression level. Preliminary analyses indicated that Ma and Mg subclasses are predominantly expressed in the inflorescences and siliques, and more meticulous studies using Affymetrix arrays showed that type I MADS box genes are expressed in male and female gametophytes as well as during early stage of endosperm and embryo development (Day et al, 2008;Walia et al, 2009;Tiwari et al, 2010;Wuest et al, 2010).The first Arabidopsis type I gene to be characterized functionally was AGL80/FEM111 (Portereiko et al, 2006), which belongs to the Mg subclade. AGL80/FEM111 is expressed in the central cell just before polar nuclei fusion, and in accordance with this observation, female gametophytes are severely affected in agl80/fem111 mutants (Schneitz et al, 1995;Christensen et al, 1997;Yadegari and Drews, 2004;Portereiko et al, 2006) (Figure 2,3).…”

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confidence: 99%

The Emerging Importance of Type I MADS Box Transcription Factors for Plant Reproduction

et al. 2011

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Based on their evolutionary origin, MADS box transcription factor genes have been divided into two classes, namely, type I and II. The plant-specific type II MIKC MADS box genes have been most intensively studied and shown to be key regulators of developmental processes, such as meristem identity, flowering time, and fruit and seed development. By contrast, very little is known about type I MADS domain transcription factors, and they have not attracted interest for a long time. A number of recent studies have now indicated a key regulatory role for type I MADS box factors in plant reproduction, in particular in specifying female gametophyte, embryo, and endosperm development. These analyses have also suggested that type I MADS box factors are decisive for setting reproductive boundaries between species. MADS DOMAIN ENCODING GENESMADS box genes are of ancient origin and are found in animals, fungi, and plants. All identified MADS box genes encode a highly conserved N-terminal DNA binding domain 55 to 60 amino acids in length named the MADS domain ( Figure 1; Trö bner et al., 1992). Homology searches in the nonredundant microbial database using a Hidden Markov Model for seed alignment of the MADS domain suggested that the MADS domain originates from the DNA binding subunit A of topoisomerases IIA subunit A (Gramzow et al., 2010).The acronym MADS ) is derived from the initials of MINICHROMOSOME MAINTENANCE1 (MCM1, Saccharomyces cerevisiae; Passmore et al., 1988), AGAMOUS (Arabidopsis thaliana; Yanofsky et al., 1990), DEFI-CIENS (Antirrhinum majus; Sommer et al., 1990), and SERUM RESPONSE FACTOR (SRF, Homo sapiens; Norman et al., 1988). These members of the MADS box gene family play important biological roles; for example, the human SRF coordinates the transcription of the proto-oncogene c-fos (Masutani et al., 1997;Mo et al., 2001), while MCM1 is central to the transcriptional control of cell type-specific genes and the pheromone response in the yeast S. cerevisiae (Shore and Sharrocks, 1995;Mead et al., 2002).Plant MADS box genes were first identified as regulators of floral organ identity and have since been reported to control additional developmental processes, such as the determination of meristem identity of vegetative, inflorescence, and floral meristems, root growth, ovule and female gametophyte development, flowering time, fruit ripening, and dehiscence (Zhang and Forde, 1998;Ng and Yanofsky, 2001;Giovannoni, 2004;Whipple et al., 2004;Liu et al., 2009). Studies using several model species, including Arabidopsis, A. majus, Petunia hybrida, Zea mays, and Oryza sativa, have revealed that many of these functions are conserved among angiosperms (Schwarz-Sommer et al., 2003;Vandenbussche et al., 2003;Kater et al., 2006). ARABIDOPSIS MADS BOX TYPE I AND TYPE II: AN EVOLUTIONARY OVERVIEWBased on sequence conservation in the MADS domain, these transcription factors can be grouped into two main lineages, named type I (SRF-like) and type II (MEF2-like; Alvarez-Buylla et al., 2000). In animals, type I genes are involv...

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Transcriptome Analysis of Proliferating Arabidopsis Endosperm Reveals Biological Implications for the Control of Syncytial Division, Cytokinin Signaling, and Gene Expression Regulation

Cited by 138 publications

References 113 publications

Integration of epigenetic and genetic controls of seed size by cytokinin in Arabidopsis

Integration of epigenetic and genetic controls of seed size by cytokinin in Arabidopsis

Global analysis of gene activity duringArabidopsisseed development and identification of seed-specific transcription factors

The Emerging Importance of Type I MADS Box Transcription Factors for Plant Reproduction

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