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Seed size is an important agronomic trait for domesticating crops. Increasing seed size is an ongoing target for improving yield. Seed development in angiosperms is launched by double fertilization within the mature ovule, which leads to the development of a diploid embryo and a triploid endosperm. The seed coat is a maternal sporophytic tissue originating from the ovule integuments. Therefore, seed size is coordinately regulated by the growth and development of the embryo, endosperm, and seed coat.
Seed coat and endosperm growth precede embryo growth during early seed development[1,2]. The seed coat not only delivers nutrients to the endosperm and embryo but also acts as the physical constraint on endosperm and embryo growth[2−4]. The growth of the endosperm, in turn, promotes elongation of the seed coat cell[4,5]. It has been proposed that the seed coat and the endosperm act coordinately to set the volume of the seed cavity for later embryonic growth and determining the seed size in Arabidopsis[2,5]. In rice and many other monocot plants, grain size is also influenced by growth of the maternal tissue spikelet hull and the endosperm[6]. Thus, the maternal tissues and endosperm play primary roles in controlling seed size. Several recent studies have demonstrated that the initiation and correct development of the seed coat depend on the endosperm rather than the embryo, and that early endosperm development is an autonomously programmed process independent of embryogenesis in Arabidopsis[7,8]. The fertilized endosperm of the embryo-free seed in Arabidopsis undergoes normal syncytium formation and cellularization as that of the wild type in terms of the cytological process and time course[7]. Additionally, an increase in coenocytic endosperm turgor pressure drives expansion of the seed[9,10]. In this case, the endosperm plays a central role in seed development and determining seed size.
Development of the nuclear endosperm is a common mechanism among angiosperms, including the monocot cereals and most dicot plants, and is characterized by the rapid proliferation of endosperm nuclei without cell division leading to the generation of a large syncytium during early endosperm development (Fig. 1a, b). Cellularization of the syncytial endosperm is initiated in the micropylar endosperm of Arabidopsis after the globular embryo stage[11]. After cellularization, endosperm cells undergo a small number of synchronous cell division depending on their position along the micropylar-chalazal axis[12]. The central portion of the peripheral endosperm undergoes cell division until the central cell cavity is completely filled with cells[12]. The endosperm then begins to break down gradually, and the reserves support early embryo development[13]. Finally, only a single peripheral endosperm cell layer, referred to as the aleurone layer, is present in the mature seed[13] (Fig. 1a). The rate of division of the cellularized endosperm is much slower than that of syncytial endosperm nuclei[1,14]. The seed almost reaches the final size at the late globular stage of embryo development[2]. Coincidence in the timing of endosperm cellularization with the end of the main stage of seed growth indicates that proliferation of the syncytial endosperm and the timing of endosperm cellularization play crucial roles in determining the sizes of the endosperm and seed in Arabidopsis and many other dicot plants[12] (Fig. 1a). The endosperm of monocot plants, such as maize and rice, occupies the most volume in the mature seed (Fig. 1b). After growth of the ephemeral syncytial endosperm, the endosperm undergoes rapid cellularization and differentiation. During this time, the cellularized endosperm also undergoes a small series of cell proliferation. Then, endoreduplication and cell expansion occur in the central part of the endosperm. Finally, the endosperm cells undergo programmed cell death (PCD) and desiccation (Fig. 1b). During the first 10 days after pollination (DAP), the proliferation of syncytial endosperm nuclei and the endosperm cell division to form the majority of the endosperm cells, which determines kernel sink strength, storage capacity, and kernel size[1,15,16] (Fig. 1b). Therefore, early endosperm growth plays a fundamental role in determining seed size in higher plants. Here, we focus on the recent advances in the regulation of early endosperm growth and discuss the possible molecular mechanisms by which early endosperm development controls seed size (Fig. 2; Table 1).
Figure 1.
Seed development in Arabidopsis and maize. (a) Schematic representation of seed development in Arabidopsis. Stages of embryo development are indicated. After fertilization, the endosperm nucleus undergoes rapid division without formation of cell walls or cytokinesis, resulting in a syncytium. Cellularization is initiated in the micropylar endosperm at the early heart embryo stage and is completed when the embryo reaches the torpedo stage. The cellularized endosperm undergoes a small series of cell proliferation until the central cell cavity is completely filled with cells. Then, the endosperm begins to breakdown, and the seed cavity is replaced by the embryo. (b) Schematic representation of seed development in B73 maize. Stages indicate days after pollination (DAP). After the syncytial endosperm proliferation and cellularization, the cellularized endosperm undergoes endoreduplication (starting at 8–10 DAP), followed by PCD (starting at about 16 DAP). The endosperm occupies the largest part of the mature kernel.
Figure 2.
Regulation of seed size by early endosperm development. Proliferation of the syncytial endosperm nuclei and the endosperm cells during early endosperm development determines the number of endosperm cells, which plays a fundamental role in the control of seed size. The red lines represent protein-protein interactions. The blue lines represent post-transcriptional regulation. The dashed lines represent unconfirmed relationships in the endosperm or in the Arabidopsis endosperm (relationships between 'AGL62', 'ATHBs', and 'YUCs or TAAs'). Abbreviations: ABA, abscisic acid; BR, brassinolide; CK, cytokinin; GA, gibberellin; PRC2, polycomb repressive complex 2.
Table 1. Genes involved in seed size control by early endosperm development.
Species Gene name Accession number Gene product Reference(s) Arabidopsis ABA2 AT1G52340 Short-chain dehydrogenase/reductase; involved in ABA biosynthesis [35] Arabidopsis ABI5 AT2G36270 bZIP transcription factor [34, 35] Arabidopsis AGL62 AT5G60440 MADS-box transcription factor [22, 23, 33,
40, 43, 44]Strawberry FveAGL62 FvH4_2g03030 MADS-box transcription factor [44] FveAGL80 FvH4_6g08460 Arabidopsis AHK2 AT5G35750 Histidine kinase; cytokinin receptor [62] AHK3 AT1G27320 AHK4 AT2G01830 Arabidopsis AHP2 AT3G29350 Histidine phosphotransfer protein; regulator of cytokinin signaling [63] AHP3 AT5G39340 AHP5 AT1G03430 Arabidopsis AIF2 AT3G06590 Non-DNA-binding bHLH transcription factor [70] Arabidopsis ARR1 AT3G16857 Transcription factor; involved in cytokinin signaling [64] ARR10 AT4G31920 ARR12 AT2G25180 Strawberry FveATHB29b FvH4_5g17830 ATHB subfamily of transcription factor [44] FveATHB30 FvH4_6g48610 Arabidopsis AXL AT2G32410 Subunit of the RUB1 activating enzyme; involved in auxin signaling [38, 39] AXR1 AT1G05180 Arabidopsis BBM AT5G17430 AP2/ERF transcription factor [25] Arabidopsis BPC1 AT2G01930 BPC transcription factor [100] BPC2 AT1G14685 Arabidopsis BZR1 AT1G75080 Transcription factor; involved in BR signaling [69] Arabidopsis CKI1 AT2G47430 Histidine kinase without cytokinin perception domain; involved in cytokinin signaling [61] Arabidopsis CKX2 AT2G19500 Cytokinin oxidase; involved in cytokinin homeostasis [27] Rice OsEMF2a Os04g08034 Polycomb group protein [53, 95] Arabidopsis FIE AT3G20740 Polycomb group protein [22, 24] Rice OsFIE1 Os08g04290 Polycomb group protein [94] Rice OsFIE2 Os08g04270 Polycomb group protein [90, 91, 93] Arabidopsis FIS2 AT2G35670 Polycomb group protein [24, 40, 43] Arabidopsis FUS3 AT3G26790 B3 domain transcription factor [100] Arabidopsis IKU1 AT2G35230 VQ motif protein [17−19, 27] Arabidopsis IKU2 AT3G19700 LRR-RLK [17, 19−21, 26, 27] Maize ZmIPT2 Zm00001d003869 Isopentenyl transferase; involved in cytokinin biosynthesis [57, 60] Arabidopsis MEA AT1G02580 Polycomb group protein [24, 43] Soybean GmMEA Gm11G067000 Polycomb group protein [26] Arabidopsis MINI3 AT1G55600 WRKY transcription factor [18−21, 27] Arabidopsis MIR159A AT1G73687 microRNA159 [31] MIR159B AT1G18075 MIR159C AT2G46255 Maize Zma-miR169o MI0013202 microRNA169o [15] Arabidopsis MSI1 AT5G58230 Polycomb group protein [24] Rice MISSEN XLOC_057324 Long noncoding RNA [32] Arabidopsis MYB33 AT5G06100 MYB transcription factor [31] MYB65 AT3G11440 Arabidopsis NAA10 AT5G13780 Catalytic subunit of Arabidopsis NatA complex [33] Arabidopsis NAA15 AT1G80410 Auxiliary subunit of Arabidopsis NatA complex [33] Maize ZmNF-YA13 Zm00001d018255 Nuclear factor Y, subunit A [15] Rice OsNF-YB1 Os02g49410 Nuclear factor Y, subunit B [46] Arabidopsis PHE1 AT1G65330 MADS-box transcription factor [96−99] Arabidopsis PLT2 AT1G51190 AP2/EREBP transcription factor [25] Arabidopsis RAN1 AT5G20010 Ras-related nuclear GTPase [34] RAN2 AT5G20020 RAN3 AT5G55190 Arabidopsis RAV1 AT1G13260 AP2/B3 domain transcription factor [76] Arabidopsis SHB1 AT4G25350 SYG1 family protein; transcription coactivator [20−22, 35] Arabidopsis TAR1 AT1G23320 Tryptophan aminotransferase; involved in auxin biosynthesis [38, 39] TAR2 AT4G24670 Arabidopsis TFL1 AT5G03840 Phosphatidylethanolamine binding protein [34] Arabidopsis WEI8 AT1G70560 Tryptophan aminotransferase; involved in auxin biosynthesis [38, 39] Maize ZmYUC1 Zm00001d023718 Flavin monooxygenase; involved in auxin biosynthesis [15, 47] Rice OsYUC11 Os12g08780 Flavin monooxygenase; involved in auxin biosynthesis [46] -
Although the early endosperm developmental period is short, it is critical to seed development. The proliferation of syncytial endosperm nuclei and the endosperm cell division that occur during early endosperm development play a crucial role in determining seed size. Substantial progress has been made in the molecular regulation of endosperm development in recent decades. However, the molecular mechanisms of early endosperm development are not clearly understood. Many important questions remain unsolved. The biochemical function of the receptor kinase IKU2 is a major puzzle in HAIKU signaling. The exact molecular functions of hormones during endosperm development and the control of seed size require additional investigations, due to the problematic pleiotropic nature of hormones. Hormonal interactions may be involved in endosperm development, such as auxin-CK interactions, ABA-BR interactions, and auxin-GA interactions. Epigenetics is involved in genome-wide regulation of imprinted and non-imprinted gene expression during early endosperm development. However, our understanding of the mechanisms of specific gene expression regulated by epigenetics during endosperm development is very limited. Biochemical approaches and new technologies, such as the single-cell/nuclear sequencing and genome editing, will be crucial for gaining clearer insight into the endosperm biology. Ultimately, a comprehensive understanding of the regulatory mechanisms of early endosperm development from basic studies will provide new guidelines and strategies to improve crops.
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Cite this article
Xu G, Zhang X. 2023. Mechanisms controlling seed size by early endosperm development. Seed Biology 2:1 doi: 10.48130/SeedBio-2023-0001
Mechanisms controlling seed size by early endosperm development
- Received: 26 October 2022
- Accepted: 19 December 2022
- Published online: 30 January 2023
Abstract: Seed size is an important agronomic trait determining the yield potential of crops that is controlled by the growth and development of the endosperm, embryo, and seed coat. The seed coat and endosperm have been proposed to play primary roles in determining seed size. Extensive research has been carried out on the regulation of seed size by seed coat, whereas the molecular mechanism underlying the regulation of seed size by the endosperm is poorly understood. Recent studies have emphasized the central role of the endosperm in seed development. The proliferation of syncytial endosperm nuclei and the endosperm cell division during early endosperm development determine the number of endosperm cells, which plays a fundamental role in controlling seed size. Here, we summarize the recent progress in early endosperm development, emphasizing the roles and molecular mechanisms of the HAIKU pathway, phytohormones, and polycomb repressive complex 2 in the control of seed size.
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Key words:
- Endosperm development /
- Seed size /
- HAIKU pathway /
- Phytohormones /
- PRC2