Evolutionarily Conserved Regulatory Mechanisms of Abscisic Acid Signaling in Land Plants: Characterization of ABSCISIC ACID INSENSITIVE1-Like Type 2C Protein Phosphatase in the Liverwort Marchantia polymorpha

Abstract

Abscisic acid (ABA) is postulated to be a ubiquitous hormone that plays a central role in seed development and responses to environmental stresses of vascular plants. However, in liverworts (Marchantiophyta), which represent the oldest extant lineage of land plants, the role of ABA has been least emphasized; thus, very little information is available on the molecular mechanisms underlying ABA responses. In this study, we isolated and characterized MpABI1, an ortholog of ABSCISIC ACID INSENSITIVE1 (ABI1), from the liverwort Marchantia polymorpha. The MpABI1 cDNA encoded a 568-amino acid protein consisting of the carboxy-terminal protein phosphatase 2C (PP2C) domain and a novel amino-terminal regulatory domain. The MpABI1 transcript was detected in the gametophyte, and its expression level was increased by exogenous ABA treatment in the gemma, whose growth was strongly inhibited by ABA. Experiments using green fluorescent protein fusion constructs indicated that MpABI1 was mainly localized in the nucleus and that its nuclear localization was directed by the aminoterminal domain. Transient overexpression of MpABI1 in M. polymorpha and Physcomitrella patens cells resulted in suppression of ABA-induced expression of the wheat Em promoter fused to the b-glucuronidase gene. Transgenic P. patens expressing MpABI1 and its mutant construct, MpABI1-d2, lacking the amino-terminal domain, had reduced freezing and osmotic stress tolerance, and associated with reduced accumulation of ABA-induced late embryogenesis abundant-like boiling-soluble proteins. Furthermore, ABA-induced morphological changes leading to brood cells were not prominent in these transgenic plants. These results suggest that MpABI1 is a negative regulator of ABA signaling, providing unequivocal molecular evidence of PP2C-mediated ABA response mechanisms functioning in liverworts.Land plants are repeatedly challenged by environmental stresses such as desiccation, salinity, and freezing, which can cause irreversible damage to intracellular structures and membranes by severe dehydration. Abscisic acid (ABA), which is known to be a phytohormone responsible for physiological control of seed maturation and germination, bud dormancy, and stomata closure, has been postulated to be involved in the development of cellular dehydration tolerance under stress conditions. In higher plants, water-stress conditions trigger a transient or sustained increase in endogenous ABA content in tissues. Increased ABA stimulates the expression of a number of stress-related genes such as those of late embryogenesis abundant (LEA) proteins, which are thought to protect cells from the damage caused by the dehydration stress (Chandler and Robertson, 1994). It has been demonstrated that various tissue-cultured cells of vascular plants, including those of angiosperms, gymnosperms, and ferns, develop desiccation and freezing tolerance upon exogenous ABA treatment, indicating that ABA plays a key role in stress tolerance at cellular

Insights into the Origin and Evolution of the Plant Hormone Signaling Machinery

“…3). Consistent with our hypothesis, the group A PP2C-mediated ABA response mechanism appears to function in M. polymorpha (Tougane et al, 2010).…”

Action of Natural Abscisic Acid Precursors and Catabolites on Abscisic Acid Receptor Complexes

“…In a search to identify orthologs of ABA signaling molecules in liverworts (Marchantia polymorpha), the earliest diverging branch of land plants, a homolog of Arabidopsis ABI1 PP2C was identified. Its function as a regulator of ABA-dependent signaling processes was found to be conserved (Tougane et al, 2010). Furthermore, a functional PP2C in the beechnut (Fagus spp.)…”

Evolution of the Stomatal Regulation of Plant Water Content

“…Whether these alternative SnRK2-independent ABA signaling pathways play an adaptively relevant role in stomatal function is yet to be determined. The core SnRK2-centric ABA signaling pathway is highly conserved across land plants with all lineages, including those species without stomata, such as liverworts, displaying functional physiological responses to ABA (Ghosh et al, 2016), RCAR/PYR/PYL ABA receptors present in genomes (Hauser et al, 2011), and functional PP2Cs (Tougane et al, 2010). This highly conserved ABA signaling pathway is known to regulate desiccation tolerance mechanisms (Tougane et al, 2010), spore dormancy, and sex determination in nonseed plants , among other processes.…”