Diverse transcriptional programs associated with environmental stress and hormones in the Arabidopsis receptor-like kinase gene family.

The genome of Arabidopsis thaliana encodes more than 600 receptor-like kinase (RLK) genes, by far the dominant class of receptors found in land plants. Although similar to the mammalian receptor tyrosine kinases, plant RLKs are serine/threonine kinases that represent a novel signaling innovation unique to plants and, consequently, an excellent opportunity to understand how extracellular signaling evolved and functions in plants as opposed to animals. RLKs are predicted to be major components of the signaling pathways that allow plants to respond to environmental and developmental conditions. However, breakthroughs in identifying these processes have been limited to only a handful of individual RLKs. Here, we used a Syngenta custom Arabidopsis GeneChip array to compile a detailed profile of the transcriptional activity of 604 receptor-like kinase genes after exposure to a cross-section of known signaling factors in plants, including abiotic stresses, biotic stresses, and hormones. In the 68 experiments comprising the study, we found that 582 of the 604 RLK genes displayed a two-fold or greater change in expression to at least one of 12 types of treatments, thereby providing a large body of experimental evidence for targeted functional screens of individual RLK genes. We investigated whether particular subfamilies of RLK genes are responsive to specific types of signals and found that each subfamily displayed broad ranges of expression, as opposed to being targeted towards particular signal classes. Finally, by analyzing the divergence of sequence and gene expression among the RLK subfamilies, we present evidence as to the functional basis for the expansion of the RLKs and how this expansion may have affected conservation and divergences in their function. Taken as a whole, our study represents a preliminary, working model of processes and interactions in which the members of the RLK gene family may be involved, where such information has remained elusive for so many of its members.

[1]  T. Boller,et al.  FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. , 2000, Molecular cell.

[2]  Xun Wang,et al.  Large-scale profiling of the Arabidopsis transcriptome. , 2000, Plant physiology.

[3]  R. Shen,et al.  Positional Signaling Mediated by a Receptor-like Kinase in Arabidopsis , 2005, Science.

[4]  S. Hazen,et al.  Gene expression profiling of plant responses to abiotic stress , 2003, Functional & Integrative Genomics.

[5]  Martin Parniske,et al.  Regulation of Plant Symbiosis Receptor Kinase through Serine and Threonine Phosphorylation* , 2005, Journal of Biological Chemistry.

[6]  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.

[7]  John C. Walker,et al.  Receptor-like protein kinases: the keys to response. , 2003, Current opinion in plant biology.

[8]  S. Shiu,et al.  Plant Receptor-Like Kinase Gene Family: Diversity, Function, and Signaling , 2001, Science's STKE.

[9]  Z. He,et al.  Requirement for the induced expression of a cell wall associated receptor kinase for survival during the pathogen response. , 1998, The Plant journal : for cell and molecular biology.

[10]  N. Tuteja,et al.  Cold, salinity and drought stresses: an overview. , 2005, Archives of biochemistry and biophysics.

[11]  A. Diévart,et al.  LRR-containing receptors regulating plant development and defense , 2003, Development.

[12]  Alan M. Jones,et al.  Plant heterotrimeric G protein function: insights from Arabidopsis and rice mutants. , 2004, Current opinion in plant biology.

[13]  Ana I. Caño-Delgado,et al.  Heterodimerization and Endocytosis of Arabidopsis Brassinosteroid Receptors BRI1 and AtSERK3 (BAK1) , 2004, The Plant Cell Online.

[14]  J. Hoch,et al.  Two-component and phosphorelay signal transduction. , 2000, Current opinion in microbiology.

[15]  A. Kereszt,et al.  A receptor kinase gene regulating symbiotic nodule development , 2002, Nature.

[16]  K. Shinozaki,et al.  Monitoring Expression Profiles of Rice Genes under Cold, Drought, and High-Salinity Stresses and Abscisic Acid Application Using cDNA Microarray and RNA Gel-Blot Analyses1[w] , 2003, Plant Physiology.

[17]  T. Vision,et al.  Divergence in expression between duplicated genes in Arabidopsis. , 2007, Molecular biology and evolution.

[18]  S. Tabata,et al.  A plant receptor-like kinase required for both bacterial and fungal symbiosis , 2002, Nature.

[19]  H. Akashi,et al.  Gene expression and molecular evolution. , 2001, Current opinion in genetics & development.

[20]  Hur-Song Chang,et al.  Toward elucidating the global gene expression patternsof developing Arabidopsis: Parallel analysis of 8 300 genesby a high-density oligonucleotide probe array , 2001 .

[21]  Ziheng Yang,et al.  PAML: a program package for phylogenetic analysis by maximum likelihood , 1997, Comput. Appl. Biosci..

[22]  D. Nicolae,et al.  Rapid divergence in expression between duplicate genes inferred from microarray data. , 2002, Trends in genetics : TIG.

[23]  F. Tax,et al.  Functional analysis of receptor-like kinases in monocots and dicots. , 2006, Current opinion in plant biology.

[24]  Hong Ma,et al.  The excess microsporocytes1 gene encodes a putative leucine-rich repeat receptor protein kinase that controls somatic and reproductive cell fates in the Arabidopsis anther. , 2002, Genes & development.

[25]  Xiaorong S. Zhang,et al.  Domain-Specific Positive Selection Contributes to the Evolution of Arabidopsis Leucine-Rich Repeat Receptor-Like Kinase (LRR RLK) Genes , 2006, Journal of Molecular Evolution.

[26]  Yudong D. He,et al.  Functional Discovery via a Compendium of Expression Profiles , 2000, Cell.

[27]  B. Kunkel,et al.  Cross talk between signaling pathways in pathogen defense. , 2002, Current opinion in plant biology.

[28]  J. Chory,et al.  BRI1 is a critical component of a plasma-membrane receptor for plant steroids , 2001, Nature.

[29]  Brody J Deyoung,et al.  The CLAVATA1-related BAM1, BAM2 and BAM3 receptor kinase-like proteins are required for meristem function in Arabidopsis. , 2006, The Plant journal : for cell and molecular biology.

[30]  Mark J. van der Laan,et al.  A new algorithm for hybrid hierarchical clustering with visualization and the bootstrap , 2003 .

[31]  Jia Li,et al.  BRL1, a leucine-rich repeat receptor-like protein kinase, is functionally redundant with BRI1 in regulating Arabidopsis brassinosteroid signaling. , 2004, The Plant journal : for cell and molecular biology.

[32]  Klaus F. X. Mayer,et al.  Comparative Analysis of the Receptor-Like Kinase Family in Arabidopsis and Rice , 2004, The Plant Cell Online.

[33]  Ralf J. Sommer,et al.  The evolution of signalling pathways in animal development , 2003, Nature Reviews Genetics.

[34]  Ann M Stock,et al.  Two-component signal transduction. , 2000, Annual review of biochemistry.

[35]  Zheng-Hui He,et al.  Antisense Expression of a Cell Wall–Associated Protein Kinase, WAK4, Inhibits Cell Elongation and Alters Morphology , 2001, The Plant Cell Online.

[36]  S. Shiu,et al.  Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[37]  Hur-Song Chang,et al.  Transcriptional Profiling Reveals Novel Interactions between Wounding, Pathogen, Abiotic Stress, and Hormonal Responses in Arabidopsis1,212 , 2002, Plant Physiology.

[38]  J. Cock,et al.  Receptor kinase signalling in plants and animals: distinct molecular systems with mechanistic similarities. , 2002, Current opinion in cell biology.

[39]  Jianming Li,et al.  BRI1/BAK1, a Receptor Kinase Pair Mediating Brassinosteroid Signaling , 2002, Cell.

[40]  S. Muse,et al.  Positively Selected Sites in the Arabidopsis Receptor-Like Kinase Gene Family , 2005, Journal of Molecular Evolution.

[41]  Ana I. Caño-Delgado,et al.  Binding of brassinosteroids to the extracellular domain of plant receptor kinase BRI1 , 2005, Nature.

[42]  J. Verica,et al.  Tissue-Specific and Developmentally Regulated Expression of a Cluster of Tandemly Arrayed Cell Wall-Associated Kinase-Like Kinase Genes in Arabidopsis1 , 2003, Plant Physiology.

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

[44]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[45]  T. Boller,et al.  Perception of the Bacterial PAMP EF-Tu by the Receptor EFR Restricts Agrobacterium-Mediated Transformation , 2006, Cell.

[46]  D. Buzas,et al.  Long-Distance Signaling in Nodulation Directed by a CLAVATA1-Like Receptor Kinase , 2002, Science.

[47]  S. D. de Vries,et al.  The Arabidopsis thaliana SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASES1 and 2 Control Male Sporogenesis , 2005, The Plant Cell Online.

[48]  S. Tabata,et al.  A receptor kinase gene of the LysM type is involved in legumeperception of rhizobial signals , 2003, Nature.

[49]  T. Hunter,et al.  Autoregulation and homodimerization are involved in the activation of the plant steroid receptor BRI1. , 2005, Developmental cell.

[50]  N. Mitsukawa,et al.  The Arabidopsis ERECTA gene encodes a putative receptor protein kinase with extracellular leucine-rich repeats. , 1996, The Plant cell.

[51]  K. Denby,et al.  Engineering drought and salinity tolerance in plants: lessons from genome-wide expression profiling in Arabidopsis. , 2005, Trends in biotechnology.

[52]  J. Good,et al.  Adaptive protein evolution and regulatory divergence in Drosophila. , 2006, Molecular biology and evolution.

[53]  T. Nomura,et al.  Cloning the Tomato Curl3 Gene Highlights the Putative Dual Role of the Leucine-Rich Repeat Receptor Kinase tBRI1/SR160 in Plant Steroid Hormone and Peptide Hormone Signaling Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.006379. , 2002, The Plant Cell Online.

[54]  Hur-Song Chang,et al.  Transcriptome Changes for Arabidopsis in Response to Salt, Osmotic, and Cold Stress1,212 , 2002, Plant Physiology.

[55]  N. King,et al.  The unicellular ancestry of animal development. , 2004, Developmental cell.

[56]  Ana I. Caño-Delgado,et al.  BRL1 and BRL3 are novel brassinosteroid receptors that function in vascular differentiation in Arabidopsis , 2004, Development.

[57]  A. Wagner,et al.  Decoupled evolution of coding region and mRNA expression patterns after gene duplication: implications for the neutralist-selectionist debate. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[58]  Todd H. Oakley,et al.  Comparative methods for the analysis of gene-expression evolution: an example using yeast functional genomic data. , 2005, Molecular biology and evolution.

[59]  B. D. Kohorn,et al.  Wall-Associated Kinases Are Expressed throughout Plant Development and Are Required for Cell Expansion , 2001, Plant Cell.

[60]  Jian-Kang Zhu,et al.  Salt and drought stress signal transduction in plants. , 2002, Annual review of plant biology.

[61]  A. Diévart,et al.  CLAVATA1 Dominant-Negative Alleles Reveal Functional Overlap between Multiple Receptor Kinases That Regulate Meristem and Organ Development Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010504. , 2003, The Plant Cell Online.

[62]  Bernardo Lemos,et al.  Evolution of proteins and gene expression levels are coupled in Drosophila and are independently associated with mRNA abundance, protein length, and number of protein-protein interactions. , 2005, Molecular biology and evolution.

[63]  Elliot M Meyerowitz,et al.  Plants Compared to Animals: The Broadest Comparative Study of Development , 2002, Science.

[64]  G. Gonnet,et al.  Exhaustive matching of the entire protein sequence database. , 1992, Science.

[65]  T. Sakurai,et al.  Monitoring the expression profiles of genes induced by hyperosmotic, high salinity, and oxidative stress and abscisic acid treatment in Arabidopsis cell culture using a full-length cDNA microarray , 2004, Plant Molecular Biology.

[66]  K. Torii,et al.  Synergistic interaction of three ERECTA-family receptor-like kinases controls Arabidopsis organ growth and flower development by promoting cell proliferation , 2004, Development.

[67]  D. McCarty,et al.  CRINKLY4: A TNFR-Like Receptor Kinase Involved in Maize Epidermal Differentiation , 1996, Science.

[68]  Hur-Song Chang,et al.  Expression Profile Matrix of Arabidopsis Transcription Factor Genes Suggests Their Putative Functions in Response to Environmental Stresses , 2002, The Plant Cell Online.

[69]  S. Tabata,et al.  Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases , 2003, Nature.

[70]  Jianzhi Zhang Evolution by gene duplication: an update , 2003 .

[71]  Fiona C. Robertson,et al.  ARABIDOPSIS CRINKLY4 Function, Internalization, and Turnover Are Dependent on the Extracellular Crinkly Repeat Domainw⃞ , 2005, The Plant Cell Online.

[72]  E. Sprinzak,et al.  Prediction of gene function by genome-scale expression analysis: prostate cancer-associated genes. , 1999, Genome research.

[73]  S. Turner,et al.  PXY, a Receptor-like Kinase Essential for Maintaining Polarity during Plant Vascular-Tissue Development , 2007, Current Biology.

[74]  Y. Matsubayashi,et al.  An LRR Receptor Kinase Involved in Perception of a Peptide Plant Hormone, Phytosulfokine , 2002, Science.

[75]  J. Bonner The origins of multicellularity , 1998 .

[76]  H. Dickinson,et al.  EXS, a Putative LRR Receptor Kinase, Regulates Male Germline Cell Number and Tapetal Identity and Promotes Seed Development in Arabidopsis , 2002, Current Biology.

[77]  Jennifer L. Nemhauser,et al.  Different Plant Hormones Regulate Similar Processes through Largely Nonoverlapping Transcriptional Responses , 2006, Cell.

[78]  M. Ohmori,et al.  HAR1 mediates systemic regulation of symbiotic organ development , 2002, Nature.

[79]  Patrik R. Jones,et al.  Allele-Specific Receptor-Ligand Interactions in Brassica Self-Incompatibility , 2022 .

[80]  Tadao Asami,et al.  Identification and Functional Analysis of in Vivo Phosphorylation Sites of the Arabidopsis BRASSINOSTEROID-INSENSITIVE1 Receptor Kinase , 2005, The Plant Cell Online.

[81]  John C. Walker,et al.  Relationship of a putative receptor protein kinase from maize to the S-locus glycoproteins of Brassica , 1990, Nature.

[82]  S. Hake,et al.  thick tassel dwarf1 encodes a putative maize ortholog of the Arabidopsis CLAVATA1 leucine-rich repeat receptor-like kinase , 2005, Development.

[83]  J. Schroeder,et al.  Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASES1 and 2 Are Essential for Tapetum Development and Microspore Maturation[W][OA] , 2005, The Plant Cell Online.

[84]  Ali S. Hadi,et al.  Finding Groups in Data: An Introduction to Chster Analysis , 1991 .

[85]  Jia Li,et al.  BAK1, an Arabidopsis LRR Receptor-like Protein Kinase, Interacts with BRI1 and Modulates Brassinosteroid Signaling , 2002, Cell.

[86]  Z. Yang,et al.  Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. , 2000, Molecular biology and evolution.

[87]  D. Kaiser,et al.  Building a multicellular organism. , 2001, Annual review of genetics.

[88]  Li-li Chen,et al.  A Receptor Kinase-Like Protein Encoded by the Rice Disease Resistance Gene, Xa21 , 1995, Science.

[89]  Wei-Hua Wu,et al.  A G Protein-Coupled Receptor Is a Plasma Membrane Receptor for the Plant Hormone Abscisic Acid , 2007, Science.

[90]  K. Torii,et al.  Dominant-Negative Receptor Uncovers Redundancy in the Arabidopsis ERECTA Leucine-Rich Repeat Receptor–Like Kinase Signaling Pathway That Regulates Organ Shape Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010413. , 2003, The Plant Cell Online.

[91]  G. Ingram,et al.  Sending the right signals: regulating receptor kinase activity. , 2005, Current opinion in plant biology.

[92]  Julia Frugoli,et al.  The Medicago truncatula SUNN Gene Encodes a CLV1-like Leucine-rich Repeat Receptor Kinase that Regulates Nodule Number and Root Length , 2005, Plant Molecular Biology.

[93]  R. Yadav,et al.  STRUBBELIG defines a receptor kinase-mediated signaling pathway regulating organ development in Arabidopsis. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[94]  Izhar Ben-Shlomo,et al.  Signaling Receptome: A Genomic and Evolutionary Perspective of Plasma Membrane Receptors Involved in Signal Transduction , 2003, Science's STKE.

[95]  Lauren M McIntyre,et al.  Common pattern of evolution of gene expression level and protein sequence in Drosophila. , 2004, Molecular biology and evolution.

[96]  Robert W. Williams,et al.  The CLAVATA1 Gene Encodes a Putative Receptor Kinase That Controls Shoot and Floral Meristem Size in Arabidopsis , 1997, Cell.

[97]  David E. Clapham,et al.  A Superfamily of Voltage-gated Sodium Channels in Bacteria* , 2004, Journal of Biological Chemistry.

[98]  K. Torii,et al.  Stomatal Patterning and Differentiation by Synergistic Interactions of Receptor Kinases , 2005, Science.

[99]  J. Stein,et al.  Molecular cloning of a putative receptor protein kinase gene encoded at the self-incompatibility locus of Brassica oleracea. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[100]  P. Becraft First published online as a Review in Advance on June 26, 2002 RECEPTOR KINASE SIGNALING IN PLANT DEVELOPMENT , 2022 .

[101]  F. Baluška,et al.  Aluminum-Induced Gene Expression and Protein Localization of a Cell Wall-Associated Receptor Kinase in Arabidopsis1 , 2003, Plant Physiology.

[102]  Robert C. Edgar,et al.  MUSCLE: multiple sequence alignment with high accuracy and high throughput. , 2004, Nucleic acids research.

[103]  Makoto Sato,et al.  The gene FLORAL ORGAN NUMBER1 regulates floral meristem size in rice and encodes a leucine-rich repeat receptor kinase orthologous to Arabidopsis CLAVATA1 , 2004, Development.