Regulation of nitrogen starvation responses by the alarmone (p)ppGpp in rice

• Published in: Journal of genetics and genomics 2022-05, Vol.49 (5), p.469-480
• Main Authors: Li, Hanwen, Nian, Jinqiang, Fang, Shuang, Guo, Meng, Huang, Xiahe, Zhang, Fengxia, Wang, Qing, Zhang, Jian, Bai, Jiaoteng, Dong, Guojun, Xin, Peiyong, Xie, Xianzhi, Chen, Fan, Wang, Guodong, Wang, Yingchun, Qian, Qian, Zuo, Jianru, Chu, Jinfang, Ma, Xiaohui
• Format: Article
• Language: English
• Subjects: (p)ppGpp; ARE2; Bacterial Proteins - genetics; Bacterial Proteins - metabolism; Chloroplasts - metabolism; Gene Expression Regulation, Bacterial; Guanosine Pentaphosphate - metabolism; Guanosine Tetraphosphate - genetics; Guanosine Tetraphosphate - metabolism; Nitrogen - metabolism; Nitrogen starvation response; Oryza - genetics; Oryza - metabolism; Plants - metabolism; Rice; Stringent response
• ISSN: 1673-8527
• DOI: 10.1016/j.jgg.2022.02.006

Nitrogen is an essential macronutrient for all living organisms and is critical for crop productivity and quality. In higher plants, inorganic nitrogen is absorbed through roots and then assimilated into amino acids by the highly conserved glutamine synthetase/glutamine:2-oxoglutarate aminotransferase (GS/GOGAT) cycle. How nitrogen metabolism and nitrogen starvation responses of plants are regulated remains largely unknown. Previous studies revealed that mutations in the rice ABNORMAL CYTOKININ RESPONSE1 (ABC1) gene encoding Fd-GOGAT cause a typical nitrogen deficiency syndrome. Here, we show that ARE2 (for ABC1 REPRESSOR2) is a key regulator of nitrogen starvation responses in rice. The are2 mutations partially rescue the nitrogen-deficient phenotype of abc1 and the are2 mutants show enhanced tolerance to nitrogen deficiency, suggesting that ARE2 genetically interacts with ABC1/Fd-GOGAT. ARE2 encodes a chloroplast-localized RelA/SpoT homolog protein that catalyzes the hydrolysis of guanosine pentaphosphate or tetraphosphate (p)ppGpp, an alarmone regulating the stringent response in bacteria under nutritional stress conditions. The are2 mutants accumulate excessive amounts of (p)ppGpp, which correlate with lower levels of photosynthetic proteins and higher amino acid levels. Collectively, these observations suggest that the alarmone (p)ppGpp mediates nitrogen stress responses and may constitute a highly conserved mechanism from bacteria to plants.