Rice NIN-LIKE PROTEIN 1 Rapidly Responds to Nitrogen Deficiency and Improves Yield and Nitrogen Use Efficiency.

Nitrogen (N) is indispensable for crop growth and yield, but excessive agricultural application of nitrogenous fertilizers has generated severe environmental problems. A desirable and economical solution to cope with these issues is to improve crop nitrogen use efficiency (NUE). Plant NUE has been a focal point of intensive research worldwide, yet much more has to be learned about its genetic determinants and regulation. Here, we show that rice NIN-LIKE PROTEIN 1 (OsNLP1) plays a fundamental role in N utilization. OsNLP1 protein localizes in nucleus and its transcript level is rapidly induced by N starvation. Overexpression of OsNLP1 improves plant growth, grain yield and NUE under different N conditions while knockout of OsNLP1 impairs grain yield and NUE under N limiting conditions. OsNLP1 regulates nitrate and ammonium utilization by cooperatively orchestrating multiple N uptake and assimilation genes. Chromatin immunoprecipitation and yeast-one-hybrid assays show that OsNLP1 can directly bind to the promoter of these genes to activate their expression. Therefore, our results demonstrate that OsNLP1 is a key regulator of N utilization and represents a potential target for improving NUE and yield in rice.

[1]  Chengcai Chu,et al.  Nitrogen-Use Divergence Between Indica and Japonica Rice: Variation at Nitrate Assimilation. , 2020, Molecular plant.

[2]  W. Terzaghi,et al.  Genome-wide associated study identifies NAC42-activated nitrate transporter conferring high nitrogen use efficiency in rice , 2019, Nature Communications.

[3]  Q. Qian,et al.  The indica nitrate reductase gene OsNR2 allele enhances rice yield potential and nitrogen use efficiency , 2019, Nature Communications.

[4]  Jie Luo,et al.  Evolutionary analyses of NIN-like proteins in plants and their roles in nitrate signaling , 2019, Cellular and Molecular Life Sciences.

[5]  Q. Xie,et al.  Nitrate–NRT1.1B–SPX4 cascade integrates nitrogen and phosphorus signalling networks in plants , 2019, Nature Plants.

[6]  Jun Lyu.  Traits enable domestication , 2019, Nature Plants.

[7]  K. Singh,et al.  Genome-wide identification and characterization of gene family for RWP-RK transcription factors in wheat (Triticum aestivum L.) , 2018, PloS one.

[8]  K. Mysore,et al.  NIN interacts with NLPs to mediate nitrate inhibition of nodulation in Medicago truncatula , 2018, Nature Plants.

[9]  Hsin-Yu Wu,et al.  Early molecular events associated with nitrogen deficiency in rice seedling roots , 2018, Scientific Reports.

[10]  Kun Wu,et al.  Modulating plant growth-metabolism coordination for sustainable agriculture , 2018, Nature.

[11]  Kun Lu,et al.  Genome-Wide Identification and Characterization of NODULE-INCEPTION-Like Protein (NLP) Family Genes in Brassica napus , 2018, International journal of molecular sciences.

[12]  Yunde Zhao,et al.  Efficient allelic replacement in rice by gene editing: A case study of the NRT1.1B gene. , 2018, Journal of integrative plant biology.

[13]  Mineko Konishi,et al.  A NIGT1-centred transcriptional cascade regulates nitrate signalling and incorporates phosphorus starvation signals in Arabidopsis , 2018, Nature Communications.

[14]  Yang Bai,et al.  Expression of the Nitrate Transporter Gene OsNRT1.1A/OsNPF6.3 Confers High Yield and Early Maturation in Rice[OPEN] , 2018, Plant Cell.

[15]  N. Crawford,et al.  Overexpression of the Maize ZmNLP6 and ZmNLP8 Can Complement the Arabidopsis Nitrate Regulatory Mutant nlp7 by Restoring Nitrate Signaling and Assimilation , 2017, Front. Plant Sci..

[16]  H. Liao,et al.  Engineering crop nutrient efficiency for sustainable agriculture. , 2017, Journal of integrative plant biology.

[17]  Chao Zhang,et al.  Discovery of nitrate–CPK–NLP signalling in central nutrient–growth networks , 2017, Nature.

[18]  D. Qi,et al.  Enhancement of cold and salt tolerance of Arabidopsis by transgenic expression of the S-adenosylmethionine decarboxylase gene from Leymus chinensis. , 2017, Journal of plant physiology.

[19]  N. Crawford,et al.  Interacting TCP and NLP transcription factors control plant responses to nitrate availability , 2017, Proceedings of the National Academy of Sciences.

[20]  E. Nambara,et al.  NIN-like protein 8 is a master regulator of nitrate-promoted seed germination in Arabidopsis , 2016, Nature Communications.

[21]  C. Xiang,et al.  Overexpression of Arabidopsis NLP7 improves plant growth under both nitrogen-limiting and -sufficient conditions by enhancing nitrogen and carbon assimilation , 2016, Scientific Reports.

[22]  Ya-ping Fu,et al.  Expanding the Range of CRISPR/Cas9 Genome Editing in Rice. , 2016, Molecular plant.

[23]  A. Iyer-Pascuzzi,et al.  The Transcription Factor NIN-LIKE PROTEIN7 Controls Border-Like Cell Release1[OPEN] , 2016, Plant Physiology.

[24]  C. Xiang,et al.  Correction: Arabidopsis ERF1 Mediates Cross-Talk between Ethylene and Auxin Biosynthesis during Primary Root Elongation by Regulating ASA1 Expression , 2016, PLoS genetics.

[25]  Rongchen Wang,et al.  The Arabidopsis NRG2 Protein Mediates Nitrate Signaling and Interacts with and Regulates Key Nitrate Regulators[OPEN] , 2016, Plant Cell.

[26]  Bin Hu,et al.  Variation in NRT1.1B contributes to nitrate-use divergence between rice subspecies , 2015, Nature Genetics.

[27]  Huifang Cen,et al.  Inside out: high-efficiency plant regeneration and Agrobacterium-mediated transformation of upland and lowland switchgrass cultivars , 2015, Plant Cell Reports.

[28]  Orli G. Bahcall.  Anopheline mosquito genomes , 2014, Nature Genetics.

[29]  T. Girin,et al.  The plant RWP-RK transcription factors: key regulators of nitrogen responses and of gametophyte development. , 2014, Journal of experimental botany.

[30]  N. von Wirén,et al.  Root Nutrient Foraging1 , 2014, Plant Physiology.

[31]  M. Hawkesford.  Reducing the reliance on nitrogen fertilizer for wheat production , 2014, Journal of cereal science.

[32]  V. Colot,et al.  Nuclear retention of the transcription factor NLP7 orchestrates the early response to nitrate in plants , 2013, Nature Communications.

[33]  Mineko Konishi,et al.  Arabidopsis NIN-like transcription factors have a central role in nitrate signalling , 2013, Nature Communications.

[34]  A. Good,et al.  Engineering nitrogen use efficient crop plants: the current status. , 2012, Plant biotechnology journal.

[35]  Guohua Xu,et al.  Plant nitrogen assimilation and use efficiency. , 2012, Annual review of plant biology.

[36]  A. Good,et al.  Biotechnological Approaches to Improving Nitrogen Use Efficiency in Plants: Alanine Aminotransferase as a Case Study , 2011 .

[37]  P. Farnham,et al.  Using ChIP-seq technology to identify targets of zinc finger transcription factors. , 2010, Methods in molecular biology.

[38]  Q. Shen,et al.  The relationship between rhizosphere nitrification and nitrogen-use efficiency in rice plants. , 2007, Plant, cell & environment.

[39]  Liangjun Da,et al.  Biodiversity changes in the lakes of the Central Yangtze , 2006 .

[40]  L. Schauser,et al.  Evolution of NIN-Like Proteins in Arabidopsis, Rice, and Lotus japonicus , 2005, Journal of Molecular Evolution.

[41]  A. Good,et al.  Can less yield more? Is reducing nutrient input into the environment compatible with maintaining crop production? , 2004, Trends in plant science.

[42]  K. Feldmann,et al.  Characterization of a chlorate-hypersensitive, high nitrate reductase Arabidopsis thaliana mutant , 1986, Theoretical and Applied Genetics.

[43]  Arsen O. Batagov,et al.  The Sym35 Gene Required for Root Nodule Development in Pea Is an Ortholog of Nin from Lotus japonicus 1 , 2003, Plant Physiology.

[44]  G. An,et al.  T-DNA Insertional Mutagenesis for Activation Tagging in Rice1 , 2002, Plant Physiology.

[45]  Leif Schauser,et al.  A plant regulator controlling development of symbiotic root nodules , 1999, Nature.

[46]  C. Foyer,et al.  Overexpression of nitrate reductase in tobacco delays drought-induced decreases in nitrate reductase activity and mRNA , 1998, Plant physiology.

[47]  R. Conrad,et al.  Denitrification coupleD to nitrification in the rhizosphere of rice , 1998 .

[48]  N. Crawford,et al.  Nitrate: nutrient and signal for plant growth. , 1995, The Plant cell.

[49]  N. Crawford,et al.  The herbicide sensitivity gene CHL1 of arabidopsis encodes a nitrate-inducible nitrate transporter , 1993, Cell.

[50]  H. Ehara,et al.  Fundamental growth response to fertilizer in rice plants. I. Varietal difference in the growth rate at the seedling stage. , 1990 .