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

Hanwen Li; Jinqiang Nian; Shuang Fang; Meng Guo; Xiahe Huang; Fengxia Zhang; Qing Wang; Jian Zhang; Jiaoteng Bai; Guojun Dong; Peiyong Xin; Xianzhi Xie; Fan Chen; Guodong Wang; Yingchun Wang; Qian Qian; Jianru Zuo; Jinfang Chu; Xiaohui Ma

doi:10.1016/j.jgg.2022.02.006

Volume 49 Issue 5

May 2022

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Article Navigation > Journal of Genetics and Genomics > 2022 > 49(5): 469-480

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

doi: 10.1016/j.jgg.2022.02.006

a State Key Laboratory of Plant Genomics, National Center for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China;
b College of Advanced Agricultural Sciences, University of Chinese Academy of Sciences, Beijing 100049, China;
c State Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China;
d Innovation Academy for Seed Design, Chinese Academy of Sciences, Beijing 100101, China;
e State Key Laboratory of Rice Biology, China National Rice Research Institute, Chinese Academy of Agricultural Sciences, Hangzhou, Zhejiang 310006, China;
f Institute of Wetland Agriculture and Ecology, Shandong Academy of Agricultural Sciences, Jinan, Shandong 250100, China;
g Hainan Yazhou Bay Laboratory, Sanya, Hainan 572025, China;
h. CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Beijing 100101, China

Funds:

We thank Michael Cashel for the (CF1648, CF1652, CF4941 and CF4943)

Ben Field for the (SAIL_391_E11)

Arizona Genomics Institute (AGI) for the BAC clone (OSJNBb0050D18). This research was supported by grants from the Ministry of Agriculture and Rural Affairs of China (2016ZX08009003-002, 2016ZX08009003-005 and 2016ZX08009003-004), Chinese Academy of Sciences (XDA08010401-2), the Ministry of Science and Technology of the People's Republic of China (2016YFD0100706), and the State Key Laboratory of Plant Genomics.

Received Date: 2021-11-21
Accepted Date: 2022-02-16
Rev Recd Date: 2022-02-14
Publish Date: 2022-02-18

Abstract

Abstract

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.
- Rice,
- Stringent response,
- Nitrogen starvation response,
- (p)ppGpp,
- ARE2

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References(62)

References

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