Current perspectives on the hormonal control of seed development in Arabidopsis and maize: a focus on auxin

Abstract

The seed represents the unit of reproduction of flowering plants, capable of developing into another plant, and to ensure the survival of the species under unfavorable environmental conditions. It is composed of three compartments: seed coat, endosperm and embryo. Proper seed development depends on the coordination of the processes that lead to seed compartments differentiation, development and maturation. The coordination of these processes is based on the constant transmission/perception of signals by the three compartments. Phytohormones constitute one of these signals; gradients of hormones are generated in the different seed compartments, and their ratios comprise the signals that induce/inhibit particular processes in seed development. Among the hormones, auxin seems to exert a central role, as it is the only one in maintaining high levels of accumulation from fertilization to seed maturation. The gradient of auxin generated by its PIN carriers affects several processes of seed development, including pattern formation, cell division and expansion. Despite the high degree of conservation in the regulatory mechanisms that lead to seed development within the Spermatophytes, remarkable differences exist during seed maturation between Monocots and Eudicots species. For instance, in Monocots the endosperm persists until maturation, and constitutes an important compartment for nutrients storage, while in Eudicots it is reduced to a single cell layer, as the expanding embryo gradually replaces it during the maturation. This review provides an overview of the current knowledge on hormonal control of seed development, by considering the data available in two model plants: Arabidopsis thaliana, for Eudicots and Zea mays L., for Monocots. We will emphasize the control exerted by auxin on the correct progress of seed development comparing, when possible, the two species.

Keywords: Arabidopsis; auxin; embryo; endosperm; maize; phytohormones; seed development.

Figure 1

Seed development in Arabidopsis and maize. (A) Schematic representation of seed development in Arabidopsis. Embryo development stages are indicated. The evolution of the endosperm is shown from the formation of the coenocyte, where the multiple anticlinal cell divisions generate nuclei placed all around the peripheral cytoplasm, followed by the formation of the peripheral endosperm layer. This layer evolves into the cellular endosperm after periclinal divisions and cell wall formation events. Later in the developmental program, the volume of the central vacuole progressively decreases to finally disappear, and the endosperm is absorbed almost completely and replaced by the growing embryo in the mature seed. At the end of maturation only three types of endosperm remain: the single-cell layered endosperm, the micropylar endosperm surrounding the embryo radicle, and the chalazal endosperm, adjacent to the chalazal cyst. (B) Schematic representation of seed development in maize. Stages indicate days after pollination (DAP). In parallel with Arabidopsis, the progression of seed development is showed from the definition of the coenocyte, to the cellularization of the endosperm and progressive disappearance of the central vacuole. The process of maturation, besides others modifications, ends with the expansion of the endosperm that finally occupies the largest part of the seed and the accumulation of starch in its cells that progressively undergo programmed cell death. (C) Schematic trend of hormone accumulation during seed development. The high level of auxin (AUX) present during all the seed development phases suggests that this hormone has a key role throughout the entire program of seed formation. The pattern of Cytokinins (CK) accumulation is the opposite with respect to auxin. CKs have a prominent role during the phase that involves cell divisions, decreasing progressively during the maturation phase, when cell expansion prevails. The brassinosteroids (BR) follow the same pattern of CKs. The highest concentration of BRs is shown at the beginning of seed development, and is detected in the maternally derived tissues (i.e., integuments). Their levels decrease at the end of maturation. The pattern of accumulation of Gibberellins (GA) is characteristic, showing two peaks corresponding to specific phases of seed development: the stage of embryo differentiation, when the GAs promote cell growth and expansion, and the end of the maturation phase, when they activate proteolytic enzymes that mobilize resources from the endosperm necessary for germination. Abscissic acid (ABA) shows an accumulation pattern complementary to the GAs, being the main hormone that inhibits all the processes induced by GAs.

Figure 2

Auxin transport during the embryogenesis development of Arabidopsis and maize. (A) Schematic representation of auxin transport during embryo development in Arabidopsis. In early embryo (one-cell stage to 16-cell stage in the figure), PIN7 (blue) is expressed in the suspensor cells localizing to the apical membranes, mediating auxin transport toward the proembryo. During the octant (not shown) and 16-cell stage, all proembryo cells express PIN1 (purple), which is evenly distributed along the inner cell membranes and not polarly localized. Later, during the transition to the globular stage, the subcellular localization of PIN1 becomes polar, facing the basal membranes. Simultaneously and similarly, the polarity of PIN7 localization is reversed, now localized at the basal membrane of suspensor cells. The localization of PIN1 and PIN7 in the basal membranes establishes an apical-basal flux of auxins that will be maintained throughout the life cycle of the plant (adapted from Friml et al., ; Weijers and Jurgens, ; Nawy et al., 2008). (B) Model for the ZmPIN1-mediated auxin transport during early stages of maize embryogenesis. Medial longitudinal sections of maize embryos at proembryo, transition and coleoptilar stages are shown. The ZmPIN1 protein (red) localizes in embryo plasma membranes. After the first division of the zygote, several cell divisions in different planes lead to the formation of the small embryo and the larger suspensor (proembryo stage). At this stage, auxins accumulate in the endosperm above the embryo but not in the embryo itself (not shown), and ZmPIN1 localizes at the cell boundaries of the undifferentiated proembryo core, without any polarity. Later, adaxial/abaxial polarity is established by the outgrowth of the scutellum at the abaxial side of the embryo (early transition stage). ZmPIN1 is polarly localized in the apical anticlinal membranes, marking the provascular cells of the differentiating scutellum, indicating an auxin flux toward the tip of the single maize cotyledon (late transition stage). At the coleoptilar stage there is the switch from apical to basal gradient of ZmPIN1, followed by a change of the auxin flux (adapted from Forestan et al., ; Chen et al., 2014). col, coleoptile; SAM, shoot apical meristem; scu, scutellum; su, suspensor. In both A and B the red arrows indicate the auxin efflux mediated by PINs.

Figure 3

Schematic representation of the factors affecting seed development in Arabidopsis and maize. Communication among seed compartments can involve one or more of the factors displayed on the right. The figure shows only the elements cited in this review. Single-headed arrows indicate regulation, double-headed arrows indicate reciprocal influence or regulation, and dashed arrows indicate an effect demonstrated only in one of the two species. Full-headed arrows indicate the communication among seed compartments.