A Complex Interplay of Tandem- and Whole-Genome Duplication Drives Expansion of the L-Type Lectin Receptor Kinase Gene Family in the Brassicaceae

The comparative analysis of plant gene families in a phylogenetic framework has greatly accelerated due to advances in next generation sequencing. In this study, we provide an evolutionary analysis of the L-type lectin receptor kinase and L-type lectin domain proteins (L-type LecRKs and LLPs) that are considered as components in plant immunity, in the plant family Brassicaceae and related outgroups. We combine several lines of evidence provided by sequence homology, HMM-driven protein domain annotation, phylogenetic analysis, and gene synteny for large-scale identification of L-type LecRK and LLP genes within nine core-eudicot genomes. We show that both polyploidy and local duplication events (tandem duplication and gene transposition duplication) have played a major role in L-type LecRK and LLP gene family expansion in the Brassicaceae. We also find significant differences in rates of molecular evolution based on the mode of duplication. Additionally, we show that LLPs share a common evolutionary origin with L-type LecRKs and provide a consistent gene family nomenclature. Finally, we demonstrate that the largest and most diverse L-type LecRK clades are lineage-specific. Our evolutionary analyses of these plant immune components provide a framework to support future plant resistance breeding.

[1]  Haiyang Wang,et al.  A gene cluster encoding lectin receptor kinases confers broad-spectrum and durable insect resistance in rice , 2014, Nature Biotechnology.

[2]  F. Govers,et al.  Phenotypic analyses of Arabidopsis T-DNA insertion lines and expression profiling reveal that multiple L-type lectin receptor kinases are involved in plant immunity. , 2014, Molecular plant-microbe interactions : MPMI.

[3]  Yu-Juan Zhong,et al.  Cucumis sativus L-type lectin receptor kinase (CsLecRK) gene family response to Phytophthora melonis, Phytophthora capsici and water immersion in disease resistant and susceptible cucumber cultivars. , 2014, Gene.

[4]  E. V. Van Damme,et al.  Lectin domains at the frontiers of plant defense , 2014, Front. Plant Sci..

[5]  Jonathan D. G. Jones,et al.  A novel approach for multi-domain and multi-gene family identification provides insights into evolutionary dynamics of disease resistance genes in core eudicot plants , 2014, bioRxiv.

[6]  Alexandros Stamatakis,et al.  RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies , 2014, Bioinform..

[7]  Wei-bo Song,et al.  A salicylic acid-induced lectin-like protein plays a positive role in the effector-triggered immunity response of Arabidopsis thaliana to Pseudomonas syringae Avr-Rpm1. , 2013, Molecular plant-microbe interactions : MPMI.

[8]  E. Lyons,et al.  Whole Genome and Tandem Duplicate Retention Facilitated Glucosinolate Pathway Diversification in the Mustard Family , 2013, Genome biology and evolution.

[9]  A. Paterson,et al.  Different patterns of gene structure divergence following gene duplication in Arabidopsis , 2013, BMC Genomics.

[10]  C. Dessimoz,et al.  Bidirectional Best Hits Miss Many Orthologs in Duplication-Rich Clades such as Plants and Animals , 2013, Genome biology and evolution.

[11]  N. Tuteja,et al.  Knights in action: lectin receptor-like kinases in plant development and stress responses. , 2013, Molecular plant.

[12]  Xun Xu,et al.  The Tarenaya hassleriana Genome Provides Insight into Reproductive Trait and Genome Evolution of Crucifers[W][OPEN] , 2013, Plant Cell.

[13]  Alan M. Moses,et al.  An atlas of over 90,000 conserved noncoding sequences provides insight into crucifer regulatory regions , 2013, Nature Genetics.

[14]  P. Singh,et al.  Lectin receptor kinases in plant innate immunity , 2013, Front. Plant Sci..

[15]  I. Dubery,et al.  Identification and Molecular Characterisation of a Lectin Receptor-like Kinase (GhLecRK-2) from Cotton , 2013, Plant Molecular Biology Reporter.

[16]  P. Reymond,et al.  Signalling of Arabidopsis thaliana response to Pieris brassicae eggs shares similarities with PAMP-triggered immunity , 2013, Journal of experimental botany.

[17]  Sebastian Proost,et al.  Gamma paleohexaploidy in the stem lineage of core eudicots: significance for MADS-box gene and species diversification. , 2012, Molecular biology and evolution.

[18]  N. Tuteja,et al.  Genome-wide analysis of lectin receptor-like kinase family from Arabidopsis and rice , 2012, Plant Molecular Biology.

[19]  P. Edger,et al.  Ancient whole genome duplications, novelty and diversification: the WGD Radiation Lag-Time Model. , 2012, Current opinion in plant biology.

[20]  T. Boller,et al.  The Lectin Receptor Kinase-VI.2 Is Required for Priming and Positively Regulates Arabidopsis Pattern-Triggered Immunity[C][W] , 2012, Plant Cell.

[21]  Maxim Teslenko,et al.  MrBayes 3.2: Efficient Bayesian Phylogenetic Inference and Model Choice Across a Large Model Space , 2012, Systematic biology.

[22]  D. Arnaud,et al.  The Arabidopsis Lectin Receptor Kinase LecRK-V.5 Represses Stomatal Immunity Induced by Pseudomonas syringae pv. tomato DC3000 , 2012, PLoS pathogens.

[23]  Stephen P. Ficklin,et al.  Modes of Gene Duplication Contribute Differently to Genetic Novelty and Redundancy, but Show Parallels across Divergent Angiosperms , 2011, PloS one.

[24]  Haibao Tang,et al.  Different Gene Families in Arabidopsis thaliana Transposed in Different Epochs and at Different Frequencies throughout the Rosids[W] , 2011, Plant Cell.

[25]  David M. Goodstein,et al.  Phytozome: a comparative platform for green plant genomics , 2011, Nucleic Acids Res..

[26]  Peer Bork,et al.  SMART 7: recent updates to the protein domain annotation resource , 2011, Nucleic Acids Res..

[27]  J. Poulain,et al.  The genome of the mesopolyploid crop species Brassica rapa , 2011, Nature Genetics.

[28]  I. Baldwin,et al.  Nicotiana attenuata LECTIN RECEPTOR KINASE1 Suppresses the Insect-Mediated Inhibition of Induced Defense Responses during Manduca sexta Herbivory[C][W] , 2011, Plant Cell.

[29]  Claude W. dePamphilis,et al.  Ancestral polyploidy in seed plants and angiosperms , 2011, Nature.

[30]  Brent S. Pedersen,et al.  Screening synteny blocks in pairwise genome comparisons through integer programming , 2011, BMC Bioinformatics.

[31]  Richard M. Clark,et al.  The Arabidopsis lyrata genome sequence and the basis of rapid genome size change , 2011, Nature Genetics.

[32]  F. Govers,et al.  The Lectin Receptor Kinase LecRK-I.9 Is a Novel Phytophthora Resistance Component and a Potential Host Target for a RXLR Effector , 2011, PLoS pathogens.

[33]  J. Poulain,et al.  The genome of Theobroma cacao , 2011, Nature Genetics.

[34]  Ari Löytynoja,et al.  webPRANK: a phylogeny-aware multiple sequence aligner with interactive alignment browser , 2010, BMC Bioinformatics.

[35]  M. Freeling,et al.  The Evolution of a High Copy Gene Array in Arabidopsis , 2010, Journal of Molecular Evolution.

[36]  F. Govers,et al.  Arabidopsis L-type lectin receptor kinases: phylogeny, classification, and expression profiles. , 2009, Journal of experimental botany.

[37]  Y. Narusaka,et al.  RRS1 and RPS4 provide a dual Resistance-gene system against fungal and bacterial pathogens. , 2009, The Plant journal : for cell and molecular biology.

[38]  A. Meyer,et al.  The evolutionary significance of ancient genome duplications , 2009, Nature Reviews Genetics.

[39]  Xuanming Liu,et al.  A Lectin Receptor Kinase Positively Regulates ABA Response During Seed Germination and Is Involved in Salt and Osmotic Stress Response , 2009, Journal of Plant Biology.

[40]  S. Gringhuis,et al.  Signalling through C-type lectin receptors: shaping immune responses , 2009, Nature Reviews Immunology.

[41]  Mikael Bodén,et al.  MEME Suite: tools for motif discovery and searching , 2009, Nucleic Acids Res..

[42]  Michael Freeling,et al.  Bias in plant gene content following different sorts of duplication: tandem, whole-genome, segmental, or by transposition. , 2009, Annual review of plant biology.

[43]  Steven Maere,et al.  Plants with double genomes might have had a better chance to survive the Cretaceous–Tertiary extinction event , 2009, Proceedings of the National Academy of Sciences.

[44]  D. Soltis,et al.  Rosid radiation and the rapid rise of angiosperm-dominated forests , 2009, Proceedings of the National Academy of Sciences.

[45]  Michael Freeling,et al.  Many or most genes in Arabidopsis transposed after the origin of the order Brassicales. , 2008, Genome research.

[46]  Kazuo Shinozaki,et al.  Large-scale collection and annotation of full-length enriched cDNAs from a model halophyte, Thellungiella halophila , 2008, BMC Plant Biology.

[47]  Guohua Yang,et al.  The Arabidopsis A4 Subfamily of Lectin Receptor Kinases Negatively Regulates Abscisic Acid Response in Seed Germination1[W][OA] , 2008, Plant Physiology.

[48]  Haibao Tang,et al.  Finding and Comparing Syntenic Regions among Arabidopsis and the Outgroups Papaya, Poplar, and Grape: CoGe with Rosids1[W] , 2008, Plant Physiology.

[49]  Robert D. Finn,et al.  InterPro: the integrative protein signature database , 2008, Nucleic Acids Res..

[50]  Stephen M. Mount,et al.  The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus) , 2008, Nature.

[51]  Dong Xu,et al.  A lectin receptor-like kinase is required for pollen development in Arabidopsis , 2008, Plant Molecular Biology.

[52]  Tanya Z. Berardini,et al.  The Arabidopsis Information Resource (TAIR): gene structure and function annotation , 2007, Nucleic Acids Res..

[53]  J. Poulain,et al.  The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla , 2007, Nature.

[54]  Ziheng Yang PAML 4: phylogenetic analysis by maximum likelihood. , 2007, Molecular biology and evolution.

[55]  Jun Li,et al.  KaKs_Calculator: Calculating Ka and Ks Through Model Selection and Model Averaging , 2007, Genom. Proteom. Bioinform..

[56]  Lars Arvestad,et al.  Evolution after gene duplication: models, mechanisms, sequences, systems, and organisms. , 2007, Journal of experimental zoology. Part B, Molecular and developmental evolution.

[57]  Carene Rizzon,et al.  Striking Similarities in the Genomic Distribution of Tandemly Arrayed Genes in Arabidopsis and Rice , 2006, PLoS Comput. Biol..

[58]  Brian C. Thomas,et al.  Following tetraploidy in an Arabidopsis ancestor, genes were removed preferentially from one homeolog leaving clusters enriched in dose-sensitive genes. , 2006, Genome research.

[59]  Thomas Mitchell-Olds,et al.  Independent Ancient Polyploidy Events in the Sister Families Brassicaceae and Cleomaceae[W] , 2006, The Plant Cell Online.

[60]  Andrew H Paterson,et al.  Buffering of crucial functions by paleologous duplicated genes may contribute cyclicality to angiosperm genome duplication. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[61]  Jeroen Raes,et al.  Nonrandom divergence of gene expression following gene and genome duplications in the flowering plant Arabidopsis thaliana , 2006, Genome Biology.

[62]  R. Gregory The evolution of the genome , 2005 .

[63]  E. Eichler,et al.  Chromosome evolution in eukaryotes: a multi-kingdom perspective. , 2005, Trends in genetics : TIG.

[64]  J. Molinier,et al.  The dual nature of homologous recombination in plants. , 2005, Trends in genetics : TIG.

[65]  Steven Salzberg,et al.  DAGchainer: a tool for mining segmental genome duplications and synteny , 2004, Bioinform..

[66]  S. Comber,et al.  Polyploidy in fishes: patterns and processes , 2004 .

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

[68]  D. Leister Tandem and segmental gene duplication and recombination in the evolution of plant disease resistance gene. , 2004, Trends in genetics : TIG.

[69]  S. Shiu,et al.  Expansion of the Receptor-Like Kinase/Pelle Gene Family and Receptor-Like Proteins in Arabidopsis1[w] , 2003, Plant Physiology.

[70]  Blake C. Meyers,et al.  Genome-Wide Analysis of NBS-LRR–Encoding Genes in Arabidopsis Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.009308. , 2003, The Plant Cell Online.

[71]  Vincent Colot,et al.  Understanding mechanisms of novel gene expression in polyploids. , 2003, Trends in genetics : TIG.

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

[73]  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.

[74]  M. Reichelt,et al.  Gene Duplication in the Diversification of Secondary Metabolism: Tandem 2-Oxoglutarate–Dependent Dioxygenases Control Glucosinolate Biosynthesis in Arabidopsis , 2001, Plant Cell.

[75]  J. Vrebalov,et al.  Self-Incompatibility in the Genus Arabidopsis: Characterization of the S Locus in the Outcrossing A. lyrata and Its Autogamous Relative A. thaliana , 2001, Plant Cell.

[76]  R. Ojeda,et al.  Discovery of tetraploidy in a mammal , 1999, Nature.

[77]  J. D. Jones,et al.  Homologues of the Cf-9 disease resistance gene (Hcr9s) are present at multiple loci on the short arm of tomato chromosome 1. , 1999, Molecular plant-microbe interactions : MPMI.

[78]  Jonathan D. G. Jones,et al.  Novel Disease Resistance Specificities Result from Sequence Exchange between Tandemly Repeated Genes at the Cf-4/9 Locus of Tomato , 1997, Cell.

[79]  H. Gerhardt,et al.  SPECIATION BY POLYPLOIDY IN TREEFROGS: MULTIPLE ORIGINS OF THE TETRAPLOID, HYLA VERSICOLOR , 1994, Evolution; international journal of organic evolution.

[80]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

[81]  F. Bakker,et al.  Molecular phylogenetics, temporal diversification, and principles of evolution in the mustard family (Brassicaceae). , 2010, Molecular biology and evolution.

[82]  D. Maddison,et al.  Mesquite: a modular system for evolutionary analysis. Version 2.6 , 2009 .

[83]  A. Rambaut TRACER v1.5 , 2009 .

[84]  D. Soltis,et al.  Polyploidy in Plants , 2005 .

[85]  Jonathan F. Wendel,et al.  Genome evolution in polyploids , 2004, Plant Molecular Biology.

[86]  Alex Bateman,et al.  The InterPro database, an integrated documentation resource for protein families, domains and functional sites , 2001, Nucleic Acids Res..

[87]  Yasuko Takahashi,et al.  Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events , 2022 .

[88]  A. Löytynoja,et al.  From The Cover: An algorithm for progressive multiple alignment of sequences with , 2022 .