Expansion and Function of Repeat Domain Proteins During Stress and Development in Plants

The recurrent repeats having conserved stretches of amino acids exists across all domains of life. Subsequent repetition of single sequence motif and the number and length of the minimal repeating motifs are essential characteristics innate to these proteins. The proteins with tandem peptide repeats are essential for providing surface to mediate protein–protein interactions for fundamental biological functions. Plants are enriched in tandem repeat containing proteins typically distributed into various families. This has been assumed that the occurrence of multigene repeats families in plants enable them to cope up with adverse environmental conditions and allow them to rapidly acclimatize to these conditions. The evolution, structure, and function of repeat proteins have been studied in all kingdoms of life. The presence of repeat proteins is particularly profuse in multicellular organisms in comparison to prokaryotes. The precipitous expansion of repeat proteins in plants is presumed to be through internal tandem duplications. Several repeat protein gene families have been identified in plants. Such as Armadillo (ARM), Ankyrin (ANK), HEAT, Kelch-like repeats, Tetratricopeptide (TPR), Leucine rich repeats (LRR), WD40, and Pentatricopeptide repeats (PPR). The structure and functions of these repeat proteins have been extensively studied in plants suggesting a critical role of these repeating peptides in plant cell physiology, stress and development. In this review, we illustrate the structural, functional, and evolutionary prospects of prolific repeat proteins in plants.

[1]  I. Small,et al.  The PPR motif - a TPR-related motif prevalent in plant organellar proteins. , 2000, Trends in biochemical sciences.

[2]  A. Harfouche,et al.  The Arabidopsis Tetratricopeptide Repeat-Containing Protein TTL1 Is Required for Osmotic Stress Responses and Abscisic Acid Sensitivity1[W] , 2006, Plant Physiology.

[3]  L. Pi,et al.  The ubiquitin ligase XBAT32 regulates lateral root development in Arabidopsis. , 2004, The Plant journal : for cell and molecular biology.

[4]  J. Coates,et al.  Armadillo repeat proteins: beyond the animal kingdom. , 2003, Trends in cell biology.

[5]  K. Medzihradszky,et al.  Arabidopsis PPR40 Connects Abiotic Stress Responses to Mitochondrial Electron Transport1[W][OA] , 2008, Plant Physiology.

[6]  M. Nieves‐Cordones,et al.  Disruption of the Arabidopsis thaliana inward-rectifier K+ channel AKT1 improves plant responses to water stress. , 2012, Plant & cell physiology.

[7]  R. Mullen,et al.  ARC1 Is an E3 Ubiquitin Ligase and Promotes the Ubiquitination of Proteins during the Rejection of Self-Incompatible Brassica Pollen Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.009845. , 2003, The Plant Cell Online.

[8]  D. Van Der Straeten,et al.  Functional analysis of SLO2 provides new insight into the role of plant PPR proteins , 2012, Plant signaling & behavior.

[9]  S. Teichmann,et al.  Domain combinations in archaeal, eubacterial and eukaryotic proteomes. , 2001, Journal of molecular biology.

[10]  D. Grierson,et al.  AtTRP1 encodes a novel TPR protein that interacts with the ethylene receptor ERS1 and modulates development in Arabidopsis , 2009, Journal of experimental botany.

[11]  Mark S. Boguski,et al.  A repeating amino acid motif in CDC23 defines a family of proteins and a new relationship among genes required for mitosis and RNA synthesis , 1990, Cell.

[12]  H. Nam,et al.  BLADE-ON-PETIOLE1 encodes a BTB/POZ domain protein required for leaf morphogenesis in Arabidopsis thaliana. , 2004, Plant & cell physiology.

[13]  Dong Liu,et al.  Functional disruption of the pentatricopeptide protein SLG1 affects mitochondrial RNA editing, plant development, and responses to abiotic stresses in Arabidopsis. , 2012, The Plant journal : for cell and molecular biology.

[14]  G. Schuster,et al.  HCF152, an Arabidopsis RNA Binding Pentatricopeptide Repeat Protein Involved in the Processing of Chloroplast psbB-psbT-psbH-petB-petD RNAs Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010397. , 2003, The Plant Cell Online.

[15]  Shanshan Zhu,et al.  Plasma membrane receptor-like kinase leaf panicle 2 acts downstream of the DROUGHT AND SALT TOLERANCE transcription factor to regulate drought sensitivity in rice , 2014, Journal of experimental botany.

[16]  C. Ponting,et al.  Eukaryotic signalling domain homologues in archaea and bacteria. Ancient ancestry and horizontal gene transfer. , 1999, Journal of molecular biology.

[17]  J. Song,et al.  ACD6, a Novel Ankyrin Protein, Is a Regulator and an Effector of Salicylic Acid Signaling in the Arabidopsis Defense Response Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.015412. , 2003, The Plant Cell Online.

[18]  M. Nieves‐Cordones,et al.  Root K(+) acquisition in plants: the Arabidopsis thaliana model. , 2011, Plant & cell physiology.

[19]  Raman Nambudripad,et al.  The ancient regulatory-protein family of WD-repeat proteins , 1994, Nature.

[20]  A. Kajava.  Structural diversity of leucine-rich repeat proteins. , 1998, Journal of molecular biology.

[21]  A. Brennicke,et al.  SLO2, a mitochondrial pentatricopeptide repeat protein affecting several RNA editing sites, is required for energy metabolism. , 2012, The Plant journal : for cell and molecular biology.

[22]  D. Goldfarb,et al.  Evolutionary specialization of the nuclear targeting apparatus. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[23]  W. Kim,et al.  Roles of Four Arabidopsis U-Box E3 Ubiquitin Ligases in Negative Regulation of Abscisic Acid-Mediated Drought Stress Responses1[C][W][OA] , 2012, Plant Physiology.

[24]  D. Goring,et al.  The diversity of plant U-box E3 ubiquitin ligases: from upstream activators to downstream target substrates. , 2009, Journal of experimental botany.

[25]  Arne Elofsson,et al.  Expansion of Protein Domain Repeats , 2006, PLoS Comput. Biol..

[26]  C. A. Thomas,et al.  Molecular cloning. , 1977, Advances in pathobiology.

[27]  She Chen,et al.  A Chaperone Function of NO CATALASE ACTIVITY1 Is Required to Maintain Catalase Activity and for Multiple Stress Responses in Arabidopsis , 2015, Plant Cell.

[28]  J. Malamy,et al.  Intrinsic and environmental response pathways that regulate root system architecture. , 2005, Plant, cell & environment.

[29]  K. Torii,et al.  Mechanisms of stomatal development. , 2012, Annual review of plant biology.

[30]  Yan Lai,et al.  Functional Analysis and Expressional Characterization of Rice Ankyrin Repeat-Containing Protein, OsPIANK1, in Basal Defense against Magnaporthe oryzae Attack , 2013, PloS one.

[31]  C. Patterson,et al.  AtCHIP, a U-Box-Containing E3 Ubiquitin Ligase, Plays a Critical Role in Temperature Stress Tolerance in Arabidopsis1 , 2003, Plant Physiology.

[32]  M. Delseny,et al.  RLK7, a leucine-rich repeat receptor-like kinase, is required for proper germination speed and tolerance to oxidative stress in Arabidopsis thaliana , 2010, Planta.

[33]  Richard D. Thompson,et al.  A Novel Plant Leucine-Rich Repeat Receptor Kinase Regulates the Response of Medicago truncatula Roots to Salt Stress[W] , 2009, The Plant Cell Online.

[34]  Jian‐Kang Zhu,et al.  Structure of a PLS-class Pentatricopeptide Repeat Protein Provides Insights into Mechanism of RNA Recognition , 2013, The Journal of Biological Chemistry.

[35]  G. Blatch,et al.  The tetratricopeptide repeat: a structural motif mediating protein-protein interactions. , 1999, BioEssays : news and reviews in molecular, cellular and developmental biology.

[36]  S. Prat,et al.  Gibberellins Signal Nuclear Import of PHOR1, a Photoperiod-Responsive Protein with Homology to Drosophila armadillo , 2001, Cell.

[37]  Dong Sub Kim,et al.  Molecular dissection of the response of a rice leucine-rich repeat receptor-like kinase (LRR-RLK) gene to abiotic stresses. , 2014, Journal of plant physiology.

[38]  Frédérique Bitton,et al.  Genome-Wide Analysis of Arabidopsis Pentatricopeptide Repeat Proteins Reveals Their Essential Role in Organelle Biogenesis , 2004, The Plant Cell Online.

[39]  Jonathan D. G. Jones,et al.  PLANT DISEASE RESISTANCE GENES. , 1997, Annual review of plant physiology and plant molecular biology.

[40]  M J Sternberg,et al.  Supersites within superfolds. Binding site similarity in the absence of homology. , 1998, Journal of molecular biology.

[41]  H. Goodman,et al.  Expression of antisense or sense RNA of an ankyrin repeat-containing gene blocks chloroplast differentiation in arabidopsis. , 1992, The Plant cell.

[42]  S. Chisholm,et al.  Host-Microbe Interactions: Shaping the Evolution of the Plant Immune Response , 2022 .

[43]  H. Leung,et al.  Spotted leaf11, a Negative Regulator of Plant Cell Death and Defense, Encodes a U-Box/Armadillo Repeat Protein Endowed with E3 Ubiquitin Ligase Activityw⃞ , 2004, The Plant Cell Online.

[44]  Hui Liao,et al.  A Plasma Membrane Receptor Kinase, GHR1, Mediates Abscisic Acid- and Hydrogen Peroxide-Regulated Stomatal Movement in Arabidopsis[W][OA] , 2012, Plant Cell.

[45]  D. Gerloff,et al.  Highly Sensitive Detection of Individual HEAT and ARM Repeats with HHpred and COACH , 2009, PloS one.

[46]  Jane P. Chang,et al.  What is a Plasma , 2003 .

[47]  Xia Li,et al.  Identification of TaWD40D, a wheat WD40 repeat-containing protein that is associated with plant tolerance to abiotic stresses , 2014, Plant Cell Reports.

[48]  M. Levitt.  Nature of the protein universe , 2009, Proceedings of the National Academy of Sciences.

[49]  P. Krishna,et al.  In Silico Identification of Carboxylate Clamp Type Tetratricopeptide Repeat Proteins in Arabidopsis and Rice As Putative Co-Chaperones of Hsp90/Hsp70 , 2010, PloS one.

[50]  Xin Li,et al.  The Ankyrin-Repeat Transmembrane Protein BDA1 Functions Downstream of the Receptor-Like Protein SNC2 to Regulate Plant Immunity1[C][OA] , 2012, Plant Physiology.

[51]  L. Lepiniec,et al.  The Arabidopsis TT2 Gene Encodes an R2R3 MYB Domain Protein That Acts as a Key Determinant for Proanthocyanidin Accumulation in Developing Seed , 2001, The Plant Cell Online.

[52]  C. James,et al.  The TRANSPARENT TESTA GLABRA1 Locus, Which Regulates Trichome Differentiation and Anthocyanin Biosynthesis in Arabidopsis, Encodes a WD40 Repeat Protein , 1999, Plant Cell.

[53]  Hong Ma,et al.  Genome‐wide Analysis of Kelch Repeat‐containing F‐box Family , 2007 .

[54]  M. V. Katti,et al.  Amino acid repeat patterns in protein sequences: Their diversity and structural‐functional implications , 2000, Protein science : a publication of the Protein Society.

[55]  S. Shiu,et al.  A Large Complement of the Predicted Arabidopsis ARM Repeat Proteins Are Members of the U-Box E3 Ubiquitin Ligase Family1[w] , 2004, Plant Physiology.

[56]  L. Lepiniec,et al.  The TT8 Gene Encodes a Basic Helix-Loop-Helix Domain Protein Required for Expression of DFR and BAN Genes in Arabidopsis Siliques , 2000, Plant Cell.

[57]  Silvio C. E. Tosatto,et al.  RAPHAEL: recognition, periodicity and insertion assignment of solenoid protein structures , 2012, Bioinform..

[58]  D. Eisenberg,et al.  A census of protein repeats. , 1999, Journal of molecular biology.

[59]  L. Laplaze,et al.  Armadillo-related proteins promote lateral root development in Arabidopsis , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[60]  Tianzhen Zhang,et al.  Molecular cloning and characterization of five genes encoding pentatricopeptide repeat proteins from Upland cotton (Gossypium hirsutum L.) , 2010, Molecular Biology Reports.

[61]  J. Deisenhofer,et al.  The leucine-rich repeat: a versatile binding motif. , 1994, Trends in biochemical sciences.

[62]  Y. Liu,et al.  Structural basis for the modular recognition of single-stranded RNA by PPR proteins , 2013, Nature.

[63]  Daniel R. Lewis,et al.  Potassium Uptake Supporting Plant Growth in the Absence of AKT1 Channel Activity , 1999, The Journal of general physiology.

[64]  Andrey V Kajava,et al.  Tandem repeats in proteins: from sequence to structure. , 2012, Journal of structural biology.

[65]  P Bork,et al.  Comparison of ARM and HEAT protein repeats. , 2001, Journal of molecular biology.

[66]  S. Kawasaki,et al.  Genetic characterization of a pentatricopeptide repeat protein gene, orf687, that restores fertility in the cytoplasmic male-sterile Kosena radish. , 2003, The Plant journal : for cell and molecular biology.

[67]  M. Nieves‐Cordones,et al.  Relative contribution of AtHAK5 and AtAKT1 to K+ uptake in the high-affinity range of concentrations. , 2008, Physiologia plantarum.

[68]  Y. Eshed,et al.  Cross Talk between Gibberellin and Cytokinin: The Arabidopsis GA Response Inhibitor SPINDLY Plays a Positive Role in Cytokinin Signaling , 2005, The Plant Cell Online.

[69]  Yong Hwa Cheong,et al.  Two calcineurin B-like calcium sensors, interacting with protein kinase CIPK23, regulate leaf transpiration and root potassium uptake in Arabidopsis. , 2007, The Plant journal : for cell and molecular biology.

[70]  Y. Ouyang,et al.  The ankyrin repeat gene family in rice: genome-wide identification, classification and expression profiling , 2009, Plant Molecular Biology.

[71]  S. van Nocker,et al.  The WD-repeat protein superfamily in Arabidopsis: conservation and divergence in structure and function , 2003, BMC Genomics.

[72]  Kai He,et al.  Genome-wide cloning and sequence analysis of leucine-rich repeat receptor-like protein kinase genes in Arabidopsis thaliana , 2010, BMC Genomics.

[73]  D. Barford,et al.  Topological characteristics of helical repeat proteins. , 1999, Current opinion in structural biology.

[74]  T. Tschaplinski,et al.  Genome-wide Identification of Lineage-specific Genes in Arabidopsis, Oryza and Populus , 2022 .

[75]  B C Meyers,et al.  Plant disease resistance genes encode members of an ancient and diverse protein family within the nucleotide-binding superfamily. , 1999, The Plant journal : for cell and molecular biology.

[76]  A. Fiser,et al.  Pentapeptide repeat proteins. , 2006, Biochemistry.

[77]  S. Bentolila,et al.  A pentatricopeptide repeat-containing gene restores fertility to cytoplasmic male-sterile plants , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[78]  K. Torii,et al.  Dysregulation of cell-to-cell connectivity and stomatal patterning by loss-of-function mutation in Arabidopsis CHORUS (GLUCAN SYNTHASE-LIKE 8) , 2010, Development.

[79]  F. Parcy,et al.  AKRP and EMB506 are two ankyrin repeat proteins essential for plastid differentiation and plant development in Arabidopsis. , 2006, The Plant journal : for cell and molecular biology.

[80]  H. Cho,et al.  CHRK1, a chitinase-related receptor-like kinase, interacts with NtPUB4, an armadillo repeat protein, in tobacco. , 2003, Biochimica et biophysica acta.

[81]  V. Betin,et al.  Ankyrin: structure, properties, and functions. , 2000, Biochemistry. Biokhimiia.

[82]  Xuhui Hong,et al.  ABA overly-sensitive 5 (ABO5), encoding a pentatricopeptide repeat protein required for cis-splicing of mitochondrial nad2 intron 3, is involved in the abscisic acid response in Arabidopsis. , 2010, The Plant journal : for cell and molecular biology.

[83]  K. Shinozaki,et al.  Isolation of Arabidopsis ahg11, a weak ABA hypersensitive mutant defective in nad4 RNA editing , 2012, Journal of experimental botany.

[84]  Y. Ouyang,et al.  Genomic survey, expression profile and co-expression network analysis of OsWD40 family in rice , 2012, BMC Genomics.

[85]  P. Puigdoménech,et al.  Ankyrin repeat-containing proteins in Arabidopsis: characterization of a novel and abundant group of genes coding ankyrin-transmembrane proteins. , 2004, Gene.

[86]  D. Ow,et al.  Stress tolerance to stress escape in plants: role of the OXS2 zinc‐finger transcription factor family , 2011, The EMBO journal.

[87]  S. Smerdon,et al.  The ankyrin repeat: a diversity of interactions on a common structural framework. , 1999, Trends in biochemical sciences.

[88]  H. Nam,et al.  The BLADE-ON-PETIOLE 1 gene controls leaf pattern formation through the modulation of meristematic activity in Arabidopsis , 2003, Development.

[89]  N. Pavletich,et al.  Structure of the p53 Tumor Suppressor Bound to the Ankyrin and SH3 Domains of 53BP2 , 1996, Science.

[90]  Andrew Bohm,et al.  Crystal structure of a GA protein βγdimer at 2.1 Å resolution , 1996, Nature.

[91]  P. Carter,et al.  Site-directed mutagenesis. , 1986, The Biochemical journal.

[92]  C. Müller,et al.  Structure of importin-β bound to the IBB domain of importin-α , 1999, Nature.

[93]  Zhongnan Yang,et al.  Roles of the nuclear-encoded chloroplast SMR domain-containing PPR protein SVR7 in photosynthesis and oxidative stress tolerance in Arabidopsis , 2014, Journal of Plant Biology.

[94]  A. Barkan,et al.  RNA Immunoprecipitation and Microarray Analysis Show a Chloroplast Pentatricopeptide Repeat Protein to Be Associated with the 5′ Region of mRNAs Whose Translation It Activatesw⃞ , 2005, The Plant Cell Online.

[95]  W. Kim,et al.  Heterologous Expression and Molecular and Cellular Characterization of CaPUB1 Encoding a Hot Pepper U-Box E3 Ubiquitin Ligase Homolog1[C] , 2006, Plant Physiology.

[96]  M. Anisimova,et al.  The evolution and function of protein tandem repeats in plants. , 2015, The New phytologist.

[97]  G. Blobel,et al.  Crystallographic Analysis of the Recognition of a Nuclear Localization Signal by the Nuclear Import Factor Karyopherin α , 1998, Cell.

[98]  M. Koornneef.  The complex syndrome of ttg mutanis , 1981 .

[99]  Alan Collmer,et al.  Pseudomonas syringae type III secretion system effectors: repertoires in search of functions. , 2009, Current opinion in microbiology.

[100]  H. Dyson,et al.  Intrinsically unstructured proteins and their functions , 2005, Nature Reviews Molecular Cell Biology.

[101]  S. Chen,et al.  An S-Domain Receptor-Like Kinase, OsSIK2, Confers Abiotic Stress Tolerance and Delays Dark-Induced Leaf Senescence in Rice1[W][OPEN] , 2013, Plant Physiology.

[102]  Jian-Min Zhou,et al.  The U-Box/ARM E3 Ligase PUB13 Regulates Cell Death, Defense, and Flowering Time in Arabidopsis1[C][W][OA] , 2012, Plant Physiology.

[103]  Adam Godzik,et al.  Strong functional patterns in the evolution of eukaryotic genomes revealed by the reconstruction of ancestral protein domain repertoires , 2011, Genome Biology.

[104]  A. Baudry,et al.  TT2, TT8, and TTG1 synergistically specify the expression of BANYULS and proanthocyanidin biosynthesis in Arabidopsis thaliana. , 2004, The Plant journal : for cell and molecular biology.

[105]  S. Swain,et al.  Genetic Analysis of Gibberellin Signal Transduction , 1996, Plant physiology.

[106]  S. Sankaranarayanan,et al.  The S-Domain Receptor Kinase Arabidopsis Receptor Kinase2 and the U Box/Armadillo Repeat-Containing E3 Ubiquitin Ligase9 Module Mediates Lateral Root Development under Phosphate Starvation in Arabidopsis1[C][W][OPEN] , 2014, Plant Physiology.

[107]  D. Gestaut,et al.  Arabidopsis emb175 and other ppr knockout mutants reveal essential roles for pentatricopeptide repeat (PPR) proteins in plant embryogenesis , 2005, Planta.

[108]  R. Kretsinger,et al.  Leucine-Rich Repeats (LRRs): Structure, Function, Evolution and Interaction with Ligands , 2005 .

[109]  S. Phillips,et al.  Crystal structure of a free radical enzyme, galactose oxidase. , 1994, Journal of molecular biology.

[110]  Silvio C. E. Tosatto,et al.  RepeatsDB: a database of tandem repeat protein structures , 2013, Nucleic Acids Res..

[111]  Vladimir N Uversky,et al.  Protein tandem repeats - the more perfect, the less structured. , 2010, The FEBS journal.

[112]  D. Stekel,et al.  AtMYB93 is a novel negative regulator of lateral root development in Arabidopsis , 2014, The New phytologist.

[113]  Ji Huang,et al.  SRWD: a novel WD40 protein subfamily regulated by salt stress in rice (OryzasativaL.). , 2008, Gene.

[114]  Andrew D. Moore,et al.  Arrangements in the modular evolution of proteins. , 2008, Trends in biochemical sciences.

[115]  W. Wooster,et al.  Crystal structure of , 2005 .

[116]  S. K. Boey,et al.  Plasma Membrane , 2005 .

[117]  D. Guttman,et al.  The Gain-of-Function Arabidopsis acd6 Mutant Reveals Novel Regulation and Function of the Salicylic Acid Signaling Pathway in Controlling Cell Death, Defenses, and Cell Growth , 1999, Plant Cell.

[118]  D. Barford,et al.  The structure of the tetratricopeptide repeats of protein phosphatase 5: implications for TPR‐mediated protein–protein interactions , 1998, The EMBO journal.

[119]  B. Dujon,et al.  Comparative Genomics and Molecular Dynamics of DNA Repeats in Eukaryotes , 2008, Microbiology and Molecular Biology Reviews.

[120]  W. Kim,et al.  Arabidopsis PUB22 and PUB23 Are Homologous U-Box E3 Ubiquitin Ligases That Play Combinatory Roles in Response to Drought Stress[W] , 2008, The Plant Cell Online.

[121]  V. Casco,et al.  PUB16 gene expression under abiotic stress and their putative role as an ARM repeat protein in Arabidopsis thaliana self-pollination pathway , 2012 .

[122]  Andrey V. Kajava,et al.  T-REKS: identification of Tandem REpeats in sequences with a K-meanS based algorithm , 2009, Bioinform..

[123]  J. Ecker,et al.  A WD40 Domain Cyclophilin Interacts with Histone H3 and Functions in Gene Repression and Organogenesis in Arabidopsis[W] , 2007, The Plant Cell Online.

[124]  Hyunjoong Kim,et al.  Functional Analysis I , 2017 .

[125]  Eric Rivals,et al.  Formation of the Arabidopsis Pentatricopeptide Repeat Family1[W] , 2006, Plant Physiology.

[126]  C. Ponting,et al.  Protein repeats: structures, functions, and evolution. , 2001, Journal of structural biology.

[127]  Chunyi Zhang,et al.  The Arabidopsis thaliana RNA editing factor SLO2, which affects the mitochondrial electron transport chain, participates in multiple stress and hormone responses. , 2014, Molecular plant.

[128]  Aaron M. Newman,et al.  XSTREAM: A practical algorithm for identification and architecture modeling of tandem repeats in protein sequences , 2007, BMC Bioinformatics.

[129]  K. Shinozaki,et al.  Leucine-Rich Repeat Receptor-Like Kinase1 Is a Key Membrane-Bound Regulator of Abscisic Acid Early Signaling in Arabidopsisw⃞ , 2005, The Plant Cell Online.

[130]  C. Grierson,et al.  The TIP GROWTH DEFECTIVE1 S-Acyl Transferase Regulates Plant Cell Growth in Arabidopsisw⃞ , 2005, The Plant Cell Online.

[131]  J. Ecker,et al.  Arabidopsis ETO1 specifically interacts with and negatively regulates type 2 1-aminocyclopropane-1-carboxylate synthases , 2005, BMC Plant Biology.

[132]  J. Schroeder,et al.  The Potassium Transporter AtHAK5 Functions in K+ Deprivation-Induced High-Affinity K+ Uptake and AKT1 K+ Channel Contribution to K+ Uptake Kinetics in Arabidopsis Roots1[w] , 2005, Plant Physiology.

[133]  H. Hamm,et al.  Crystal structure of a G-protein beta gamma dimer at 2.1A resolution. , 1996, Nature.

[134]  M. Nasrallah,et al.  A Cryptic Modifier Causing Transient Self-Incompatibility in Arabidopsis thaliana , 2007, Current Biology.

[135]  Srinivasan,et al.  Cloning and characterization of a pentatricopeptide protein encoding gene (LOJ) that is specifically expressed in lateral organ junctions in Arabidopsis thaliana. , 2005, Gene.

[136]  C. Bond,et al.  Selection patterns on restorer-like genes reveal a conflict between nuclear and mitochondrial genomes throughout angiosperm evolution , 2011, Proceedings of the National Academy of Sciences.

[137]  Crucial roles of the pentatricopeptide repeat protein SOAR1 in Arabidopsis response to drought, salt and cold stresses , 2015, Plant Molecular Biology.

[138]  H. Berman,et al.  The future of the Protein Data Bank. , 2013, Biopolymers.

[139]  Brody J Deyoung,et al.  Plant NBS-LRR proteins in pathogen sensing and host defense , 2006, Nature Immunology.

[140]  Erich Bornberg-Bauer,et al.  The Dynamics and Evolutionary Potential of Domain Loss and Emergence , 2011, Molecular biology and evolution.

[141]  Xinnian Dong,et al.  Characterization of an Arabidopsis Mutant That Is Nonresponsive to Inducers of Systemic Acquired Resistance. , 1994, The Plant cell.

[142]  P. Tompa.  Intrinsically unstructured proteins. , 2002, Trends in biochemical sciences.

[143]  Arabidopsis leucine-rich repeat extensin (LRX) proteins modify cell wall composition and influence plant growth , 2015, BMC Plant Biology.

[144]  Synan F. AbuQamar,et al.  The Arabidopsis Mitochondria-Localized Pentatricopeptide Repeat Protein PGN Functions in Defense against Necrotrophic Fungi and Abiotic Stress Tolerance1[C][W][OA] , 2011, Plant Physiology.

[145]  X. Qiu,et al.  ANKYRIN REPEAT-CONTAINING PROTEIN 2A Is an Essential Molecular Chaperone for Peroxisomal Membrane-Bound ASCORBATE PEROXIDASE3 in Arabidopsis[W][OA] , 2010, Plant Cell.

[146]  I. C. Lee,et al.  Age-dependent action of an ABA-inducible receptor kinase, RPK1, as a positive regulator of senescence in Arabidopsis leaves. , 2011, Plant & cell physiology.

[147]  L. Cattolico,et al.  Identification of the fertility restoration locus, Rfo, in radish, as a member of the pentatricopeptide‐repeat protein family , 2003 .

[148]  Erich Bornberg-Bauer,et al.  Evidence of interaction network evolution by whole-genome duplications: a case study in MADS-box proteins. , 2006, Molecular biology and evolution.

[149]  Markus Gruber,et al.  REPPER—repeats and their periodicities in fibrous proteins , 2005, Nucleic Acids Res..

[150]  W. Kim,et al.  CHRK1, a chitinase-related receptor-like kinase, plays a role in plant development and cytokinin homeostasis in tobacco , 2003, Plant Molecular Biology.

[151]  N. Khan.  Site-Directed Mutagenesis , 2017 .

[152]  I. Hwang,et al.  AKR2A-mediated import of chloroplast outer membrane proteins is essential for chloroplast biogenesis , 2008, Nature Cell Biology.

[153]  I. Karube,et al.  Identification and characterization of mRNA transcripts differentially expressed in response to high salinity by means of differential display in the mangrove, Bruguiera gymnorrhiza , 2002 .

[154]  R. Bahadur,et al.  The DNA-binding activity of an AP2 protein is involved in transcriptional regulation of a stress-responsive gene, SiWD40, in foxtail millet. , 2012, Genomics.

[155]  J. Mundy,et al.  Knockout of Arabidopsis accelerated-cell-death11 encoding a sphingosine transfer protein causes activation of programmed cell death and defense. , 2002, Genes & development.

[156]  S. Chen,et al.  Receptor-like kinase OsSIK1 improves drought and salt stress tolerance in rice (Oryza sativa) plants. , 2010, The Plant journal : for cell and molecular biology.

[157]  P. Bork.  Hundreds of ankyrin‐like repeats in functionally diverse proteins: Mobile modules that cross phyla horizontally? , 1993, Proteins.

[158]  H. Bohnert,et al.  Involvement of Arabidopsis HOS15 in histone deacetylation and cold tolerance , 2008, Proceedings of the National Academy of Sciences.

[159]  Brody J Deyoung,et al.  BAM Receptors Regulate Stem Cell Specification and Organ Development Through Complex Interactions With CLAVATA Signaling , 2008, Genetics.

[160]  J. Chory,et al.  A Putative Leucine-Rich Repeat Receptor Kinase Involved in Brassinosteroid Signal Transduction , 1997, Cell.

[161]  S. H. Kim,et al.  SRFR1, a suppressor of effector-triggered immunity, encodes a conserved tetratricopeptide repeat protein with similarity to transcriptional repressors. , 2009, The Plant journal : for cell and molecular biology.

[162]  Amarjeet Singh,et al.  Comprehensive Expression Analysis of Rice Armadillo Gene Family During Abiotic Stress and Development , 2014, DNA research : an international journal for rapid publication of reports on genes and genomes.

[163]  Jane Glazebrook,et al.  The Arabidopsis NPR1 Gene That Controls Systemic Acquired Resistance Encodes a Novel Protein Containing Ankyrin Repeats , 1997, Cell.

[164]  M. Sussman,et al.  A role for the AKT1 potassium channel in plant nutrition. , 1998, Science.

[165]  Jinfa F. Zhang,et al.  The radish Rfo restorer gene of Ogura cytoplasmic male sterility encodes a protein with multiple pentatricopeptide repeats. , 2003, The Plant journal : for cell and molecular biology.

[166]  L. Cooley,et al.  The kelch repeat superfamily of proteins: propellers of cell function. , 2000, Trends in cell biology.

[167]  Pamela C Ronald,et al.  Rice XA21 Binding Protein 3 Is a Ubiquitin Ligase Required for Full Xa21-Mediated Disease Resistance[W][OA] , 2006, The Plant Cell Online.