Modulating plant growth-metabolism coordination for sustainable agriculture

Enhancing global food security by increasing the productivity of green revolution varieties of cereals risks increasing the collateral environmental damage produced by inorganic nitrogen fertilizers. Improvements in the efficiency of nitrogen use of crops are therefore essential; however, they require an in-depth understanding of the co-regulatory mechanisms that integrate growth, nitrogen assimilation and carbon fixation. Here we show that the balanced opposing activities and physical interactions of the rice GROWTH-REGULATING FACTOR 4 (GRF4) transcription factor and the growth inhibitor DELLA confer homeostatic co-regulation of growth and the metabolism of carbon and nitrogen. GRF4 promotes and integrates nitrogen assimilation, carbon fixation and growth, whereas DELLA inhibits these processes. As a consequence, the accumulation of DELLA that is characteristic of green revolution varieties confers not only yield-enhancing dwarfism, but also reduces the efficiency of nitrogen use. However, the nitrogen-use efficiency of green revolution varieties and grain yield are increased by tipping the GRF4–DELLA balance towards increased GRF4 abundance. Modulation of plant growth and metabolic co-regulation thus enables novel breeding strategies for future sustainable food security and a new green revolution.The balance of DELLA and GRF4 proteins in plants ensures the co-regulation of growth with metabolism and tipping this balance towards GRF4 leads to higher efficiency of nitrogen use.

[1]  Yujing Wang,et al.  Firefly Luciferase Complementation Imaging Assay for Protein-Protein Interactions in Plants1[C][W][OA] , 2007, Plant Physiology.

[2]  Wei Liu,et al.  A Robust CRISPR/Cas9 System for Convenient, High-Efficiency Multiplex Genome Editing in Monocot and Dicot Plants. , 2015, Molecular plant.

[3]  Qian Qian,et al.  Natural variation at the DEP1 locus enhances grain yield in rice , 2009, Nature Genetics.

[4]  Steven L Salzberg,et al.  HISAT: a fast spliced aligner with low memory requirements , 2015, Nature Methods.

[5]  Qian Liu,et al.  Shedding light on integrative GA signaling. , 2014, Current opinion in plant biology.

[6]  J. Morgan,et al.  Leaf Anatomy and Gas Exchange in Nearly Isogenic Semidwarf and Tall Winter Wheat , 1989 .

[7]  Yuejin Wu,et al.  Non-canonical regulation of SPL transcription factors by a human OTUB1-like deubiquitinase defines a new plant type rice associated with higher grain yield , 2017, Cell Research.

[8]  Qian Liu,et al.  Heterotrimeric G proteins regulate nitrogen-use efficiency in rice , 2014, Nature Genetics.

[9]  Wen-Yao Liu,et al.  Do phosphorus nutrition and iron plaque alter arsenate (As) uptake by rice seedlings in hydroponic culture , 2004 .

[10]  Colin N. Dewey,et al.  RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome , 2011, BMC Bioinformatics.

[11]  R. A. Donahue,et al.  Leaf Orientation of Soybean Seedlings: II. Receptor Sites and Light Stimuli , 1990 .

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

[13]  M. Matsuoka,et al.  The Gibberellin Signaling Pathway Is Regulated by the Appearance and Disappearance of SLENDER RICE1 in Nuclei Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010319. , 2002, The Plant Cell Online.

[14]  Li-hong Xie,et al.  A Rare Allele of GS2 Enhances Grain Size and Grain Yield in Rice. , 2015, Molecular plant.

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

[16]  Mark Stitt,et al.  Metabolic and signaling aspects underpinning the regulation of plant carbon nitrogen interactions. , 2010, Molecular plant.

[17]  P. Christou,et al.  ‘Green revolution’ genes encode mutant gibberellin response modulators , 1999, Nature.

[18]  K. Chong,et al.  OsMADS57 together with OsTB1 coordinates transcription of its target OsWRKY94 and D14 to switch its organogenesis to defense for cold adaptation in rice , 2018, The New phytologist.

[19]  M. Sauter,et al.  Differential expression of a CAK (cdc2-activating kinase)-like protein kinase, cyclins and cdc2 genes from rice during the cell cycle and in response to gibberellin. , 1997, The Plant journal : for cell and molecular biology.

[20]  Prabhu L Pingali,et al.  Green Revolution: Impacts, limits, and the path ahead , 2012, Proceedings of the National Academy of Sciences.

[21]  Lixing Yuan,et al.  Additive contribution of AMT1;1 and AMT1;3 to high-affinity ammonium uptake across the plasma membrane of nitrogen-deficient Arabidopsis roots. , 2006, The Plant journal : for cell and molecular biology.

[22]  G. S. Khush,et al.  Green revolution: A mutant gibberellin-synthesis gene in rice , 2002, Nature.

[23]  R. Evenson,et al.  Assessing the Impact of the Green Revolution, 1960 to 2000 , 2003, Science.

[24]  Qian Liu,et al.  The OsSPL16-GW7 regulatory module determines grain shape and simultaneously improves rice yield and grain quality , 2015, Nature Genetics.

[25]  Peter Hedden,et al.  The genes of the Green Revolution. , 2003, Trends in genetics : TIG.

[26]  Mike Merrick,et al.  Molecular Basis and Regulation of Ammonium Transporter in Rice , 2009 .

[27]  G. Khush.  Green revolution: preparing for the 21st century. , 1999, Genome.

[28]  M. Umeda,et al.  The cell cycle genes cycA1;1 and cdc2Os-3 are coordinately regulated by gibberellin in planta , 2000, Planta.

[29]  Cole Trapnell,et al.  Ultrafast and memory-efficient alignment of short DNA sequences to the human genome , 2009, Genome Biology.

[30]  M. Gooding,et al.  Effect of wheat dwarfing genes on nitrogen-use efficiency , 2011, The Journal of Agricultural Science.

[31]  Y. Tsay,et al.  CHL1 Functions as a Nitrate Sensor in Plants , 2009, Cell.

[32]  M. Ellis,et al.  Semidwarf (sd-1), “green revolution” rice, contains a defective gibberellin 20-oxidase gene , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[33]  Siu-Ming Yiu,et al.  SOAP2: an improved ultrafast tool for short read alignment , 2009, Bioinform..

[34]  Qian Qian,et al.  Control of grain size, shape and quality by OsSPL16 in rice , 2012, Nature Genetics.

[35]  T. Yamaya,et al.  Assimilation of ammonium ions and reutilization of nitrogen in rice (Oryza sativa L.). , 2007, Journal of experimental botany.

[36]  Ruthie Angelovici,et al.  Detection of protein-protein interactions in plants using bimolecular fluorescence complementation. , 2004, The Plant journal : for cell and molecular biology.

[37]  Antonio Serrano-Mislata,et al.  DELLA genes restrict inflorescence meristem function independently of plant height , 2017, Nature Plants.

[38]  J. Peng,et al.  The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses. , 1997, Genes & development.

[39]  Qian Qian,et al.  Genome-Wide Binding Analysis of the Transcription Activator IDEAL PLANT ARCHITECTURE1 Reveals a Complex Network Regulating Rice Plant Architecture[W] , 2013, Plant Cell.

[40]  Y. Benjamini,et al.  Controlling the false discovery rate in behavior genetics research , 2001, Behavioural Brain Research.

[41]  M. Yamasaki,et al.  Artificial selection for a green revolution gene during japonica rice domestication , 2011, Proceedings of the National Academy of Sciences.

[42]  R. L. Warner,et al.  Synthesis and degradation of barley nitrate reductase. , 1983, Plant physiology.

[43]  N. Harberd,et al.  The Angiosperm Gibberellin-GID1-DELLA Growth Regulatory Mechanism: How an “Inhibitor of an Inhibitor” Enables Flexible Response to Fluctuating Environments , 2009, The Plant Cell Online.

[44]  W. Shi,et al.  Nitrogen runoff dominates water nitrogen pollution from rice-wheat rotation in the Taihu Lake region of China , 2012 .

[45]  Sir Gordon Conway.  One Billion Hungry , 2012 .

[46]  Xu-dong Zhu,et al.  Regulation of OsGRF4 by OsmiR396 controls grain size and yield in rice , 2015, Nature Plants.

[47]  Jiaqiang Sun,et al.  Haplotype variation of Green Revolution gene Rht-D1 during wheat domestication and improvement. , 2014, Journal of integrative plant biology.

[48]  Bin Hu,et al.  Control of grain size and rice yield by GL2-mediated brassinosteroid responses , 2015, Nature Plants.

[49]  X. Wang,et al.  OsLG3 contributing to rice grain length and yield was mined by Ho-LAMap , 2017, BMC Biology.