Multilayered Regulation of Membrane-Bound ONAC054 Is Essential for Abscisic Acid-Induced Leaf Senescence in Rice

ONAC054 promotes ABA-induced leaf senescence, and its activity is regulated through alternative 3′ splice site selection and cleavage of a C-terminal transmembrane domain. In most plants, abscisic acid (ABA) induces premature leaf senescence; however, the mechanisms of ABA signaling during leaf senescence remain largely unknown. Here, we show that the rice (Oryza sativa) NAM/ATAF1/2/CUC2 (NAC) transcription factor ONAC054 plays an important role in ABA-induced leaf senescence. The onac054 knockout mutants maintained green leaves, while ONAC054-overexpressing lines showed early leaf yellowing under dark- and ABA-induced senescence conditions. Genome-wide microarray analysis showed that ABA signaling-associated genes, including ABA INSENSITIVE5 (OsABI5) and senescence-associated genes, including STAY-GREEN and NON-YELLOW COLORING1 (NYC1), were significantly down-regulated in onac054 mutants. Chromatin immunoprecipitation and protoplast transient assays showed that ONAC054 directly activates OsABI5 and NYC1 by binding to the mitochondrial dysfunction motif in their promoters. ONAC054 activity is regulated by proteolytic processing of the C-terminal transmembrane domain (TMD). We found that nuclear import of ONAC054 requires cleavage of the putative C-terminal TMD. Furthermore, the ONAC054 transcript (termed ONAC054α) has an alternatively spliced form (ONAC054β), with seven nucleotides inserted between intron 5 and exon 6, truncating ONAC054α protein at a premature stop codon. ONAC054β lacks the TMD and thus localizes to the nucleus. These findings demonstrate that the activity of ONAC054, which is important for ABA-induced leaf senescence in rice, is precisely controlled by multilayered regulatory processes.

[1]  S. Yanagisawa,et al.  Multilayered Regulation of Membrane-Bound ONAC054 Is Essential for Abscisic Acid-Induced Leaf Senescence in Rice. , 2020, The Plant cell.

[2]  H. Nam,et al.  Leaf Senescence: Systems and Dynamics Aspects. , 2019, Annual review of plant biology.

[3]  G. An,et al.  Rice transcription factor OsMYB102 delays leaf senescence by down-regulating abscisic acid accumulation and signaling , 2019, Journal of experimental botany.

[4]  Hongwei Guo,et al.  Genetic redundancy of senescence-associated transcription factors in Arabidopsis. , 2018, Journal of experimental botany.

[5]  Eun-Young Kim,et al.  Roles of rice PHYTOCHROME-INTERACTING FACTOR-LIKE1 (OsPIL1) in leaf senescence , 2017, Plant signaling & behavior.

[6]  Feng Ming,et al.  A Rice NAC Transcription Factor Promotes Leaf Senescence via ABA Biosynthesis1[OPEN] , 2017, Plant Physiology.

[7]  H. Nam,et al.  Regulatory network of NAC transcription factors in leaf senescence. , 2016, Current opinion in plant biology.

[8]  B. Kuai,et al.  ABF2, ABF3, and ABF4 Promote ABA-Mediated Chlorophyll Degradation and Leaf Senescence by Transcriptional Activation of Chlorophyll Catabolic Genes and Senescence-Associated Genes in Arabidopsis. , 2016, Molecular plant.

[9]  Su-Hyun Han,et al.  Mutation of Rice Early Flowering3.1 (OsELF3.1) delays leaf senescence in rice , 2016, Plant Molecular Biology.

[10]  Nobutaka Mitsuda,et al.  The NAC transcription factor ANAC046 is a positive regulator of chlorophyll degradation and senescence in Arabidopsis leaves , 2016, Scientific Reports.

[11]  Sudhir Kumar,et al.  MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. , 2016, Molecular biology and evolution.

[12]  F. Myouga,et al.  SNAC-As, stress-responsive NAC transcription factors, mediate ABA-inducible leaf senescence. , 2015, The Plant journal : for cell and molecular biology.

[13]  G. An,et al.  Rice ONAC106 Inhibits Leaf Senescence and Increases Salt Tolerance and Tiller Angle. , 2015, Plant & cell physiology.

[14]  B. Kuai,et al.  Jasmonic acid promotes degreening via MYC2/3/4- and ANAC019/055/072-mediated regulation of major chlorophyll catabolic genes. , 2015, The Plant journal : for cell and molecular biology.

[15]  Junxian He,et al.  PHYTOCHROME-INTERACTING FACTOR 5 (PIF5) positively regulates dark-induced senescence and chlorophyll degradation in Arabidopsis. , 2015, Plant science : an international journal of experimental plant biology.

[16]  B. Kuai,et al.  EIN3 and ORE1 Accelerate Degreening during Ethylene-Mediated Leaf Senescence by Directly Activating Chlorophyll Catabolic Genes in Arabidopsis , 2015, PLoS genetics.

[17]  Su-Hyun Han,et al.  The Arabidopsis Transcription Factor NAC016 Promotes Drought Stress Responses by Repressing AREB1 Transcription through a Trifurcate Feed-Forward Regulatory Loop Involving NAP[OPEN] , 2015, Plant Cell.

[18]  Gynheung An,et al.  Mutation of Oryza sativa CORONATINE INSENSITIVE 1b (OsCOI1b) delays leaf senescence. , 2015, Journal of integrative plant biology.

[19]  S. Munné-Bosch,et al.  Transcription Factor ATAF1 in Arabidopsis Promotes Senescence by Direct Regulation of Key Chloroplast Maintenance and Senescence Transcriptional Cascades1[OPEN] , 2015, Plant Physiology.

[20]  G. Choi,et al.  Phytochrome-interacting transcription factors PIF4 and PIF5 induce leaf senescence in Arabidopsis , 2014, Nature Communications.

[21]  Yana Zhu,et al.  OsNAP connects abscisic acid and leaf senescence by fine-tuning abscisic acid biosynthesis and directly targeting senescence-associated genes in rice , 2014, Proceedings of the National Academy of Sciences.

[22]  Su-Hyun Han,et al.  Mutation of the Arabidopsis NAC016 transcription factor delays leaf senescence. , 2013, Plant & cell physiology.

[23]  Simon R. Law,et al.  The Membrane-Bound NAC Transcription Factor ANAC013 Functions in Mitochondrial Retrograde Regulation of the Oxidative Stress Response in Arabidopsis[C][W] , 2013, Plant Cell.

[24]  Simon R. Law,et al.  A Membrane-Bound NAC Transcription Factor, ANAC017, Mediates Mitochondrial Retrograde Signaling in Arabidopsis[W][OPEN] , 2013, Plant Cell.

[25]  S. Gan,et al.  Salicylic acid 3-hydroxylase regulates Arabidopsis leaf longevity by mediating salicylic acid catabolism , 2013, Proceedings of the National Academy of Sciences.

[26]  R. Tanaka,et al.  Stay-green plants: what do they tell us about the molecular mechanism of leaf senescence , 2013, Photosynthesis Research.

[27]  B. Glick,et al.  Strategies to ameliorate abiotic stress-induced plant senescence , 2013, Plant Molecular Biology.

[28]  T. Beeckman,et al.  Lateral Root Development , 2013 .

[29]  Mi Jung Kim,et al.  Controlled nuclear import of the transcription factor NTL6 reveals a cytoplasmic role of SnRK2.8 in the drought-stress response. , 2012, The Biochemical journal.

[30]  Yamile Marquez,et al.  Alternative splicing in plants – coming of age , 2012, Trends in plant science.

[31]  Chung-Mo Park,et al.  A NAC transcription factor NTL4 promotes reactive oxygen species production during drought-induced leaf senescence in Arabidopsis. , 2012, The Plant journal : for cell and molecular biology.

[32]  B. Mueller‐Roeber,et al.  Overproduction of chl B retards senescence through transcriptional reprogramming in Arabidopsis. , 2012, Plant & cell physiology.

[33]  Yuge Li,et al.  A highly efficient rice green tissue protoplast system for transient gene expression and studying light/chloroplast-related processes , 2011, Plant Methods.

[34]  K. Mishiba,et al.  Arabidopsis IRE1 catalyses unconventional splicing of bZIP60 mRNA to produce the active transcription factor , 2011, Scientific reports.

[35]  Mineko Konishi,et al.  The regulatory region controlling the nitrate-responsive expression of a nitrate reductase gene, NIA1, in Arabidopsis. , 2011, Plant & cell physiology.

[36]  Shoshi Kikuchi,et al.  Genome-wide analysis of NAC transcription factor family in rice. , 2010, Gene.

[37]  Chung-Mo Park,et al.  A membrane-bound NAC transcription factor as an integrator of biotic and abiotic stress signals , 2010, Plant signaling & behavior.

[38]  Randeep Rakwal,et al.  The NAC transcription factor RIM1 of rice is a new regulator of jasmonate signaling. , 2010, The Plant journal : for cell and molecular biology.

[39]  K. Shinozaki,et al.  Potential utilization of NAC transcription factors to enhance abiotic stress tolerance in plants by biotechnological approach , 2010, GM crops.

[40]  Qi Xie,et al.  Dual function of Arabidopsis ATAF1 in abiotic and biotic stress responses , 2009, Cell Research.

[41]  Hisashi Ito,et al.  Participation of Chlorophyll b Reductase in the Initial Step of the Degradation of Light-harvesting Chlorophyll a/b-Protein Complexes in Arabidopsis* , 2009, The Journal of Biological Chemistry.

[42]  Daehee Hwang,et al.  Trifurcate Feed-Forward Regulation of Age-Dependent Cell Death Involving miR164 in Arabidopsis , 2009, Science.

[43]  Z. Avramova,et al.  An efficient chromatin immunoprecipitation (ChIP) protocol for studying histone modifications in Arabidopsis plants , 2008, Nature Protocols.

[44]  Fang Zhang,et al.  A bZIP transcription factor, OsABI5, is involved in rice fertility and stress tolerance , 2008, Plant Molecular Biology.

[45]  A. Fernie.  Faculty Opinions recommendation of Genome-wide analysis of mRNA decay rates and their determinants in Arabidopsis thaliana. , 2008 .

[46]  S. Howell,et al.  An Endoplasmic Reticulum Stress Response in Arabidopsis Is Mediated by Proteolytic Processing and Nuclear Relocation of a Membrane-Associated Transcription Factor, bZIP28[W][OA] , 2007, The Plant Cell Online.

[47]  R. Breaker,et al.  Riboswitch Control of Gene Expression in Plants by Splicing and Alternative 3′ End Processing of mRNAs[W][OA] , 2007, The Plant Cell Online.

[48]  J. Sheen,et al.  Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis , 2007, Nature Protocols.

[49]  A. To,et al.  The Arabidopsis ABA-deficient mutant aba4 demonstrates that the major route for stress-induced ABA accumulation is via neoxanthin isomers. , 2007, The Plant journal : for cell and molecular biology.

[50]  Hisashi Ito,et al.  Rice NON-YELLOW COLORING1 Is Involved in Light-Harvesting Complex II and Grana Degradation during Leaf Senescence[W] , 2007, The Plant Cell Online.

[51]  X. Xu,et al.  Plastid transformation in the monocotyledonous cereal crop, rice (Oryza sativa) and transmission of transgenes to their progeny. , 2006, Molecules and cells.

[52]  C. Pikaard,et al.  Gateway-compatible vectors for plant functional genomics and proteomics. , 2006, The Plant journal : for cell and molecular biology.

[53]  K. Skriver,et al.  DNA-binding specificity and molecular functions of NAC transcription factors , 2005 .

[54]  Tieyan Liu,et al.  Transcription Factors in Rice: A Genome-wide Comparative Analysis between Monocots and Eudicots , 2005, Plant Molecular Biology.

[55]  Xing Wang Deng,et al.  Genome-Wide ORFeome Cloning and Analysis of Arabidopsis Transcription Factor Genes1[w] , 2004, Plant Physiology.

[56]  S. Mangan,et al.  Structure and function of the feed-forward loop network motif , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[57]  U. Grossniklaus,et al.  A Gateway Cloning Vector Set for High-Throughput Functional Analysis of Genes in Planta[w] , 2003, Plant Physiology.

[58]  Filip Rolland,et al.  Role of the Arabidopsis Glucose Sensor HXK1 in Nutrient, Light, and Hormonal Signaling , 2003, Science.

[59]  Thomas D. Schmittgen,et al.  Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. , 2001, Methods.

[60]  N. Chua,et al.  Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. , 2000, Genes & development.

[61]  R. Amasino,et al.  Diverse range of gene activity during Arabidopsis thaliana leaf senescence includes pathogen-independent induction of defense-related genes , 1999, Plant Molecular Biology.

[62]  P. Busk,et al.  Regulation of abscisic acid-induced transcription , 1998, Plant Molecular Biology.

[63]  T. Kuroiwa,et al.  Three-dimensional analysis of the senescence program in rice (Oryza sativa L.) coleoptiles , 1998, Planta.

[64]  H Fujisawa,et al.  Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant. , 1997, The Plant cell.

[65]  M. Koornneef,et al.  Biochemical Characterization of the aba2 and aba3 Mutants in Arabidopsis thaliana , 1997, Plant physiology.

[66]  J. Mol,et al.  The No Apical Meristem Gene of Petunia Is Required for Pattern Formation in Embryos and Flowers and Is Expressed at Meristem and Primordia Boundaries , 1996, Cell.

[67]  R. J. Porra,et al.  Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy , 1989 .

[68]  N. Paek,et al.  Salt Treatments and Induction of Senescence. , 2018, Methods in molecular biology.

[69]  Su-Hyun Han,et al.  Arabidopsis NAC016 promotes chlorophyll breakdown by directly upregulating STAYGREEN1 transcription , 2015, Plant Cell Reports.

[70]  S. Munné-Bosch,et al.  Transcription Factor ATAF 1 in Arabidopsis Promotes Senescence by Direct Regulation of Key Chloroplast Maintenance and Senescence Transcriptional Cascades 1 [ OPEN ] , 2015 .

[71]  S. Katsuma,et al.  Two short-chain dehydrogenase/reductases, NON-YELLOW COLORING 1 and NYC1-LIKE, are required for chlorophyll b and light-harvesting complex II degradation during senescence in rice. , 2009, The Plant journal : for cell and molecular biology.

[72]  S. Howell,et al.  An Endoplasmic Reticulum Stress Response in Arabidopsis Is Mediated by Proteolytic Processing and Nuclear Relocation of a Membrane-Associated Transcription Factor , bZIP 28 , 2008 .

[73]  S. Howell,et al.  An Endoplasmic Reticulum Stress Response in Arabidopsis Is Mediated by Proteolytic Processing and Nuclear Relocation of a Membrane-Associated Transcription Factor, bZIP28 , 2007 .

[74]  H. Nam,et al.  Leaf senescence. , 2007, Annual review of plant biology.

[75]  K. Shinozaki,et al.  Isolation and Functional Analysis of Arabidopsis Stress-Inducible NAC Transcription Factors That Bind to a Drought-Responsive cis-Element in the early responsive to dehydration stress 1 Promoter , 2004 .

[76]  Steven,et al.  Biochemical Characterization of the aba 2 and aba 3 Mutants in Arabidopsis fhaliana ’ , 2002 .

[77]  Thomas D. Schmittgen,et al.  Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2 2 DD C T Method , 2022 .