Abstract
Programmed cell death (PCD) in multicellular organisms is a vital process in growth, development, and stress responses that contributes to the formation of tissues and organs. Although numerous studies have defined the molecular participants in apoptotic and PCD cascades, successful identification of early master regulators that target specific cells to live or die is limited. Using Zea mays somatic embryogenesis as a model system, we report that the expressions of two plant hemoglobin (Hb) genes (ZmHb1 and ZmHb2) regulate the cell survival/death decision that influences somatic embryogenesis through their cell-specific localization patterns. Suppression of either of the two ZmHbs is sufficient to induce PCD through a pathway initiated by elevated NO and Zn2+ levels and mediated by production of reactive oxygen species. The effect of the death program on the fate of the developing embryos is dependent on the localization patterns of the two ZmHbs. During somatic embryogenesis, ZmHb2 transcripts are restricted to a few cells anchoring the embryos to the subtending embryogenic tissue, whereas ZmHb1 transcripts extend to several embryonic domains. Suppression of ZmHb2 induces PCD in the anchoring cells, allowing the embryos to develop further, whereas suppression of ZmHb1 results in massive PCD, leading to abortion. We conclude that regulation of the expression of these ZmHbs has the capability to determine the developmental fate of the embryogenic tissue during somatic embryogenesis through their effect on PCD. This unique regulation might have implications for development and differentiation in other species.
Highlights
Programmed cell death (PCD) in multicellular organisms is a vital process in growth, development, and stress responses that contributes to the formation of tissues and organs
In many plant species, including maize, an obligatory event of this process is the differentiation of immature somatic embryos from the surface of the embryogenic tissue consisting of a heterogeneous cell population
This differentiation step is facilitated by removal of plant growth regulators (Fig. 1A), and in spruce, it requires the selective elimination of embryogenic cells through PCD (Filonova et al, 2000)
Summary
Programmed cell death (PCD) in multicellular organisms is a vital process in growth, development, and stress responses that contributes to the formation of tissues and organs. The effect of the death program on the fate of the developing embryos is dependent on the localization patterns of the two ZmHbs. During somatic embryogenesis, ZmHb2 transcripts are restricted to a few cells anchoring the embryos to the subtending embryogenic tissue, whereas ZmHb1 transcripts extend to several embryonic domains. This unique regulation might have implications for development and differentiation in other species. Execution of PCD has been reported during different phases of the plant life cycle It establishes polarity in immature embryos, it eliminates suspensor cells in mature embryos, it contributes to the formation of vascular tissue throughout development, and it is involved in senescence-related processes (Reape et al, 2008). In spruce (Picea abies), the activation of PCD is an obligatory step for the formation of somatic embryos, and experimental suppression of the death program compromises embryogenesis (for review, see Bozhkov et al, 2005)
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