Arabidopsis plastid AMOS1/EGY1 integrates abscisic acid signaling to regulate global gene expression response to ammonium stress.
Ammonium (NH(4)(+)) is a ubiquitous intermediate of nitrogen metabolism but is notorious for its toxic effects on most organisms. Extensive studies of the underlying mechanisms of NH(4)(+) toxicity have been reported in plants, but it is poorly understood how plants acclimate to high levels of NH(4)(+). Here, we identified an Arabidopsis (Arabidopsis thaliana) mutant, ammonium overly sensitive1 (amos1), that displays severe chlorosis under NH(4)(+) stress. Map-based cloning shows amos1 to carry a mutation in EGY1 (for ethylene-dependent, gravitropism-deficient, and yellow-green-like protein1), which encodes a plastid metalloprotease. Transcriptomic analysis reveals that among the genes activated in response to NH(4)(+), 90% are regulated dependent on AMOS1/EGY1. Furthermore, 63% of AMOS1/EGY1-dependent NH(4)(+)-activated genes contain an ACGTG motif in their promoter region, a core motif of abscisic acid (ABA)-responsive elements. Consistent with this, our physiological, pharmacological, transcriptomic, and genetic data show that ABA signaling is a critical, but not the sole, downstream component of the AMOS1/EGY1-dependent pathway that regulates the expression of NH(4)(+)-responsive genes and maintains chloroplast functionality under NH(4)(+) stress. Importantly, abi4 mutants defective in ABA-dependent and retrograde signaling, but not ABA-deficient mutants, mimic leaf NH(4)(+) hypersensitivity of amos1. In summary, our findings suggest that an NH(4)(+)-responsive plastid retrograde pathway, which depends on AMOS1/EGY1 function and integrates with ABA signaling, is required for the regulation of expression of NH(4)(+)-responsive genes that maintain chloroplast integrity in the presence of high NH(4)(+) levels.
State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing 210008, China.
Baohai
B
Li
Qing
Q
Li
Liming
L
Xiong
Herbert J
HJ
Kronzucker
Ute
U
Krämer
Weiming
W
Shi
D000040:Abscisic Acid / Q000378:metabolism* / Q000494:pharmacology; D017360:Arabidopsis / Q000187:drug effects / Q000235:genetics / Q000502:physiology*; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D020869:Gene Expression Profiling; D018506:Gene Expression Regulation, Plant / Q000187:drug effects*; D017343:Genes, Plant / Q000235:genetics; D056426:Genetic Loci / Q000235:genetics; D006861:Hydrogen Peroxide / Q000494:pharmacology; D045726:Metalloproteases / Q000235:genetics / Q000378:metabolism*; D009154:Mutation / Q000235:genetics; D018087:Plastids / Q000187:drug effects / Q000378:metabolism; D000644:Quaternary Ammonium Compounds / Q000633:toxicity*; D012333:RNA, Messenger / Q000235:genetics / Q000378:metabolism; D015398:Signal Transduction / Q000187:drug effects / Q000235:genetics*; D013312:Stress, Physiological / Q000187:drug effects / Q000235:genetics*; D014158:Transcription, Genetic / Q000187:drug effects
D029681:Arabidopsis Proteins; D000644:Quaternary Ammonium Compounds; D012333:RNA, Messenger; D000040:Abscisic Acid; D006861:Hydrogen Peroxide; C500788:EGY1 protein, Arabidopsis; D045726:Metalloproteases