Phytoglobins regulate nitric oxide-dependent abscisic acid synthesis and ethylene-induced program cell death in developing maize somatic embryos

Abstract

During maize somatic embryogenesis, suppression of phytoglobins (Pgbs) reduced ABA levels leading to ethylene-induced programmed cell death in the developing embryos. These effects modulate embryonic yield depending on the cellular localization of specific phytoglobin gene expression. Suppression of Zea mays phytoglobins (ZmPgb1.1 or ZmPgb1.2) during somatic embryogenesis induces programmed cell death (PCD) by elevating nitric oxide (NO). While ZmPgb1.1 is expressed in many embryonic domains and its suppression results in embryo abortion, ZmPgb1.2 is expressed in the basal cells anchoring the embryos to the embryogenic tissue. Down-regulation of ZmPgb1.2 is required to induce PCD in these anchor cells allowing the embryos to develop further. Exogenous applications of ABA could reverse the effects caused by the suppression of either of the two ZmPgbs. A depletion of ABA, ascribed to a down-regulation of biosynthetic genes, was observed in those embryonic domains where the respective ZmPgbs were repressed. These effects were mediated by NO. Depletion in ABA content increased the transcription of genes participating in the synthesis and response of ethylene, as well as the accumulation of ethylene, which influenced embryogenesis. Somatic embryo number was reduced by high ethylene levels and increased with pharmacological treatments suppressing ethylene synthesis. The ethylene inhibition of embryogenesis was linked to the production of reactive oxygen species (ROS) and the execution of PCD. Integration of ABA and ethylene in the ZmPgb regulation of embryogenesis is proposed in a model where NO accumulates in ZmPgb-suppressing cells, decreasing the level of ABA. Abscisic acid inhibits ethylene biosynthesis and the NO-mediated depletion of ABA relieves this inhibition causing ethylene to accumulate. Elevated ethylene levels trigger production of ROS and induce PCD. Ethylene-induced PCD in the ZmPgb1.1-suppressing line [ZmPgb1.1 (A)] leads to embryo abortion, while PCD in the ZmPgb1.2-suppressing line [ZmPgb1.2 (A)] results in the elimination of the anchor cells and the successful development of the embryos.

Initiation and Execution of Programmed Cell Death and Regulation of Reactive Oxygen Species in Plants

“…ABA is a positive regulator of the senescence process, and ABA levels increase in senescing leaves, which is accompanied by the increased expression of the genes encoding the key enzymes involved in ABA biosynthesis [ 80 , 81 ]. In maize, the appropriate onset and progression of PCD in the endosperm depend on the balance between ABA and ethylene; treating the wild type with an inhibitor of ABA biosynthesis phenocopied ABA-deficient mutants, including an increase in ethylene production and accelerated execution of PCD [ 82 ].…”

Plant hemoglobins: a journey from unicellular green algae to vascular plants

“…Physiological work using transgenic plants with altered concentrations of Glbs has shown that these proteins play an important role in plant development and morphogenesis, and largely supports the theory that they do so by modulating NO concentrations (Hill, ; Hebelstrup et al , ). Glbs may act through NO modulation to affect the signaling pathways of hormones including auxins (Elhiti et al , ), cytokinins (Ross et al , ; Wang et al , ), salicylate (Mur et al , ), jasmonates (Mur et al , ; Mira et al , ), ethylene (Mur et al , ; Kapoor et al , ; Hartman et al , ) and abscisic acid (ABA; Kapoor et al , ; Rubio et al , ). Two exemplary studies, concerning the response of Arabidopsis to biotic and abiotic stress, will illustrate the triple crosstalk between Glbs, hormones and NO.…”

Genome-wide identification, evolution and expression analysis of the aspartic protease gene family during rapid growth of moso bamboo (Phyllostachys edulis) shoots

“…SCW-and PCD-related cis-elements were also found upstream of PhAP57.1, − 57.2 and − 57.3 ( Figure S1). To date, methyl jasmonate (MeJA)-, gibberellin (GA)-, ABA-, and ethylene-related as well as MYB transcription factors have been reported to be involved in PCD [58][59][60]. Hence, these results suggested that PhAPs may be potentially involved in SCW and PCD processes.…”