ABSTRACT
Aluminum (Al) toxicity and low pH are major factors limiting plant growth in acidic soils. Sensitive to Proton Rhizotoxicity 1 (STOP1) transcription factors respond to these stresses by regulating the expression of multiple Al- or low pH-responsive genes. ZmSTOP1-A, a STOP1-like protein from maize (Zea mays), was localized to the nucleus and showed transactivation activity. ZmSTOP1-A was expressed moderately in both roots and shoots of maize seedlings, but was not induced by Al stress or low pH. Overexpression of ZmSTOP1-A in Arabidopsis Atstop1 mutant partially restored Al tolerance and improved low pH tolerance with respect to root growth. Regarding Al tolerance, ZmSTOP1-A/Atstop1 plants showed clear upregulation of organic acid transporter genes, leading to increased organic acid secretion and reduced Al accumulation in roots. In addition, the antioxidant enzyme activity in roots and shoots of ZmSTOP1-A/Atstop1 plants was significantly enhanced, ultimately alleviating Al toxicity via scavenging reactive oxygen species. Similarly, ZmSTOP1-A could directly activate ZmMATE1 expression in maize, positively correlated with the number of Al-responsive GGNVS cis-elements in the ZmMATE1 promoter. Our results reveal that ZmSTOP1-A is an important transcription factor conferring Al tolerance by enhancing organic acid secretion and reactive oxygen species scavenging in Arabidopsis.
Subject(s)
Arabidopsis Proteins , Arabidopsis , Arabidopsis/metabolism , Arabidopsis Proteins/genetics , Arabidopsis Proteins/metabolism , Reactive Oxygen Species/metabolism , Aluminum/toxicity , Aluminum/metabolism , Plant Roots/genetics , Plant Roots/metabolism , Transcription Factors/genetics , Transcription Factors/metabolism , Gene Expression Regulation, PlantABSTRACT
A previous metabolomic and genome-wide association analysis of maize screened a glucose-6-phosphate 1-epimerase (ZmG6PE) gene, which responds to low-phosphorus (LP) stress and regulates yield in maize's recombinant inbred lines (RILs). However, the relationship of ZmG6PE with phosphorus and yield remained elusive. This study aimed to elucidate the underlying response mechanism of the ZmG6PE gene to LP stress and its consequential impact on maize yield. The analysis indicated that ZmG6PE required the Aldose_epim conserved domain to maintain enzyme activity and localized in the nucleus and cell membrane. The zmg6pe mutants showed decreased biomass and sugar contents but had increased starch content in leaves under LP stress conditions. Combined transcriptome and metabolome analysis showed that LP stress activated plant immune regulation in response to the LP stress through carbon metabolism, amino acid metabolism, and fatty acid metabolism. Notably, LP stress significantly reduced the synthesis of glucose-1-phosphate, mannose-6-phosphate, and ß-alanine-related metabolites and changed the expression of related genes. ZmG6PE regulates LP stress by mediating the expression of ZmSPX6 and ZmPHT1.13. Overall, this study revealed that ZmG6PE affected the number of grains per ear, ear thickness, and ear weight under LP stress, indicating that ZmG6PE participates in the phosphate signaling pathway and affects maize yield-related traits through balancing carbohydrates homeostasis.
ABSTRACT
Aluminum (Al) toxicity causes severe reduction in crop yields in acidic soil. The natural resistance-associated macrophage proteins (NRAMPs) play an important role in the transport of mineral elements in plants. Recently, OsNrat1 and SbNrat1 were reported specifically to transport trivalent Al ions. In this study, we functionally characterized ZmNRAMP4, a gene previously identified from RNA-Seq data from Al-treated maize roots, in response to Al exposure in maize. ZmNRAMP4 was predominantly expressed in root tips and was specifically induced by Al stress. Yeast cells expressing ZmNRAMP4 were hypersensitive to Al, which was associated with Al accumulation in yeast. Furthermore, overexpression of ZmNRAMP4 in Arabidopsis conferred transgenic plants with a significant increase in Al tolerance. However, expression of ZmNRAMP4, either in yeast or in Arabidopsis, had no effect on the response to cadmium stress. Taken together, these results underlined an internal tolerance mechanism involving ZmNRAMP4 to enhance Al tolerance via cytoplasmic sequestration of Al in maize.
Subject(s)
Arabidopsis , Aluminum/metabolism , Arabidopsis/genetics , Arabidopsis/metabolism , Gene Expression Regulation, Plant , Plant Proteins/metabolism , Plant Roots/metabolism , Plants, Genetically Modified/genetics , Saccharomyces cerevisiae/genetics , Saccharomyces cerevisiae/metabolism , Zea mays/genetics , Zea mays/metabolismABSTRACT
Aluminum (Al) toxicity is the main factor limiting plant growth and the yield of cereal crops in acidic soils. Al-induced oxidative stress could lead to the excessive accumulation of reactive oxygen species (ROS) and aldehydes in plants. Aldehyde dehydrogenase (ALDH) genes, which play an important role in detoxification of aldehydes when exposed to abiotic stress, have been identified in most species. However, little is known about the function of this gene family in the response to Al stress. Here, we identified an ALDH gene in maize, ZmALDH, involved in protection against Al-induced oxidative stress. Al stress up-regulated ZmALDH expression in both the roots and leaves. The expression of ZmALDH only responded to Al toxicity but not to other stresses including low pH and other metals. The heterologous overexpression of ZmALDH in Arabidopsis increased Al tolerance by promoting the ascorbate-glutathione cycle, increasing the transcript levels of antioxidant enzyme genes as well as the activities of their products, reducing MDA, and increasing free proline synthesis. The overexpression of ZmALDH also reduced Al accumulation in roots. Taken together, these findings suggest that ZmALDH participates in Al-induced oxidative stress and Al accumulation in roots, conferring Al tolerance in transgenic Arabidopsis.
