Team effort: Combinatorial control of seed maturation by transcription factors
Introduction
Seed development encompasses a series of sequential physio-morphological changes, which are often orchestrated by a network of transcription factors (TFs) [1]. Two major phases of seed development are the establishment of the basic body pattern during early embryogenesis and seed maturation. These processes depend on the spatiotemporal regulation of TFs, a feature crucial for multicellular organisms to exert sophisticated control of gene expression [2]. The coordination of TFs allows for the control of major maturation events in orthodox seeds that can withstand desiccation and freezing temperatures. These events include storage reserve accumulation, chlorophyll degradation, and the acquisition of primary dormancy, desiccation tolerance (DT), and longevity [1,3,4]. Storage reserve accumulation begins in early maturation. Seeds are filled with seed storage proteins (SSPs), oil, and storage polysaccharides, which later serve as energy sources for germinative growth [1,4]. Chlorophyll degradation begins in late maturation to reduce the production of reactive oxygen species and phototoxic products [3,5,6]. This is crucial for the acquisition of DT and longevity, as dehydrated embryos lack active metabolisms to relieve oxidative stress [7, 8, 9]. Dehydration occurs in late maturation to prepare embryos for entry into the dry state of glassy cytoplasm and immobilized biomolecules [4,8]. The collapse of cells and damaging of biomolecules during dehydration can be prevented by storage compounds, non-reducing sugars, and late embryogenesis abundant (LEA) proteins [4,6,9]. Seed germination in adverse environments is avoided by primary or secondary dormancy, which has been reviewed extensively [3,10, 11, 12]. Successful completion of the maturation programs also helps to maintain seed longevity and vigor [8,9,13]. The sequential events of seed maturation often rely on the recruitment of distinct sets of TFs and chromatin modifiers to the regulatory regions of target genes. In the following, we summarize regulatory commonalities across major maturation traits, and discuss TF-mediated coordination of the complex process during seed maturation.
Section snippets
Combinatorial regulation through the LAFL master TFs
The transcription of genes encoding the master regulators of seed development, LEAFY COTYLEDON 1 (LEC1), ABA INSENSITIVE 3 (ABI3), FUSCA 3 (FUS3), and LEC2, is tightly regulated. Collectively, these genes are known as the LAFL TFs. Recent reviews discussed how the LAFL factors form a regulatory network to govern all major traits during seed maturation [14,15]. LEC1 encodes the NF-YB subunit of the NF–Y complex, which binds to CCAAT cis-regulatory elements (CREs) in target genes. ABI3, FUS3, and
Combinatorial TF regulation of specific traits
In this section, we provide examples of extensive combinatorial regulation by TFs and the recruitment of repressive machineries in regulating specific maturation traits.
Impact of abscisic acid on TF regulation and seed maturation
Developmental and environmental cues may affect transcription through phytohormones. Abscisic acid (ABA) is a phytohormone induced during mid-embryogenesis and is essential for seed maturation [3]. Seeds of severe ABA signaling mutants are nondormant, desiccation intolerant, and contain less seed storage reserve [3]. The importance of ABA produced in the endosperm for dormancy has been well established using dry or imbibed seeds [81, 82, 83]. Recently, characterization of the ABA biosynthesis
Prospects
The examples summarized so far demonstrate important features of TF networks, including the combinatorial function of TFs and chromatin modifications, regulatory cascades, and transcriptional feedback. Here, we list several research directions to advance our understanding of transcriptional networks during seed maturation.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this article.
Acknowledgements
The authors apologize to authors of literature whose work could not be included because of page limitations. This work was funded by UBC Four Year Doctoral Fellowship (4YF) to M.A., BC Graduate Scholarship to R.H., and NSERC RGPIN-2019-05039 to L.S. They thank Sonia Gazzarrini for a stimulating discussion on the manuscript.
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Genomic imprinting regulates establishment and release of seed dormancy
2022, Current Opinion in Plant BiologyCitation Excerpt :Nevertheless, genome-wide epigenetic profiles of the endosperm during germination are required to fully understand the dynamics of epigenetic modifications and their consequences on seed dormancy. Seed dormancy is a critical trait for both wild plants and agricultural crops, and epigenetic regulators take a central position in establishing and releasing seed dormancy [49,50]. Epigenetic effects regulating seed dormancy take place in the endosperm, a unique seed tissue with parental-specific gene expression patterns throughout its development [16,30].
The Arabidopsis transcription factors AtPHL1 and AtHB23 act together promoting carbohydrate transport from pedicel-silique nodes to seeds
2022, Plant ScienceCitation Excerpt :Notably, SWEET11 has been described as essential for grain filling in rice plants [85,86] in agreement with the results reported here. Interestingly, the regulation of seed development comprising storage reserve accumulation, dormancy, desiccation tolerance, and longevity was proposed as a coordinated function of multiple TFs and not a task of an individual one [87]. Moreover, a significant number of interactions between TFs belonging to different TF families have recently been reviewed [88].
Transcriptomic Profiling of Embryogenic and Non-Embryogenic Callus Provides New Insight into the Nature of Recalcitrance in Cannabis
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These authors contributed equally to this work.