The plant-specific SCL30a SR protein regulates ABA-dependent seed traits and salt stress tolerance during germination

Abstract

SR (serine/arginine-rich) proteins are conserved RNA-binding proteins best known as key regulators of splicing, which have also been implicated in other steps of gene expression. Despite mounting evidence for their role in plant development and stress responses, the molecular pathways underlying SR protein regulation of these processes remain elusive. Here we show that the plant-specific SCL30a SR protein negatively regulates abscisic acid (ABA) signaling to control important seed traits and salt stress responses during germination in Arabidopsis. The SCL30a gene is upregulated during seed imbibition and germination, and its loss of function results in smaller seeds displaying enhanced dormancy and elevated expression of ABA-responsive genes as well as of genes repressed during the germination process. Moreover, the knockout mutant is hypersensitive to ABA and high salinity, while transgenic plants overexpressing SCL30a exhibit reduced ABA sensitivity and enhanced tolerance to salt stress during seed germination. An ABA biosynthesis inhibitor rescues the mutants enhanced sensitivity to stress, and epistatic analyses confirm that this hypersensitivity requires a functional ABA pathway. Finally, seed ABA levels are unchanged by altered SCL30a expression, indicating that the SR protein positively regulates stress tolerance during seed germination by reducing sensitivity to the phytohormone. Our results reveal a new key player in ABA-mediated control of early development and stress response, and underscore the role of plant SR proteins as important regulators of the ABA signaling pathway. Author SummarySeed germination is a critical step in plant development determining the transition to aerial growth and exposure to a more challenging environment. As such, seeds have evolved mechanisms that prevent germination under adverse conditions, thereby increasing the chances of plant survival. As a general regulator of plant development and a key mediator of stress responses, the hormone abscisic acid (ABA) promotes a prolonged non-germinating state called dormancy, influences seed size and represses germination under environmental stress. Here, we show that an RNA-binding protein, SCL30a, controls seed size, dormancy, germination and tolerance to high salinity in the model plant Arabidopsis thaliana. Loss of SCL30a gene function results in smaller and more dormant seeds with reduced ability to germinate in a high-salt environment; by contrast, SCL30a overexpression produces larger seeds that germinate faster under salt stress. Using a large-scale gene expression analysis, we identify the ABA hormonal pathway as a putative target of SCL30a. We then use genetic and pharmacological tools to unequivocally demonstrate that the uncovered biological functions of SCL30a are achieved through modulation of the ABA pathway. Our study reveals a novel regulator of key seed traits and has biotechnological implications for crop improvement under adverse environments.