Paleo-evolutionary plasticity of plant disease resistance genes

BMC Genomics

Jerome Salse¹  Thierry Langin¹  Caroline Pont¹  Florent Murat¹  Rongzhi Zhang² 

[1] INRA/UBP UMR 1095 GDEC ‘Génétique, Diversité et Ecophysiologie des Céréales’, 5 chemin de Beaulieu, 63100 Clermont-Ferrand, France;Institute of Crop Sciences, Shandong Academy of Agricultural Sciences, Jinan 250100, China

关键词: Evolution;    Plasticity;    Duplication;    R-genes;   

Others  :  1217806
DOI  :  10.1186/1471-2164-15-187

 received in 2013-09-05, accepted in 2014-02-25,  发布年份 2014

【 摘 要 】

Background

The recent access to a large set of genome sequences, combined with a robust evolutionary scenario of modern monocot (i.e. grasses) and eudicot (i.e. rosids) species from their founder ancestors, offered the opportunity to gain insights into disease resistance genes (R-genes) evolutionary plasticity.

Results

We unravel in the current article (i) a R-genes repertoire consisting in 7883 for monocots and 15758 for eudicots, (ii) a contrasted R-genes conservation with 23.8% for monocots and 6.6% for dicots, (iii) a minimal ancestral founder pool of 384 R-genes for the monocots and 150 R-genes for the eudicots, (iv) a general pattern of organization in clusters accounting for more than 60% of mapped R-genes, (v) a biased deletion of ancestral duplicated R-genes between paralogous blocks possibly compensated by clusterization, (vi) a bias in R-genes clusterization where Leucine-Rich Repeats act as a ‘glue’ for domain association, (vii) a R-genes/miRNAs interome enriched toward duplicated R-genes.

Conclusions

Together, our data may suggest that R-genes family plasticity operated during plant evolution (i) at the structural level through massive duplicates loss counterbalanced by massive clusterization following polyploidization; as well as at (ii) the regulation level through microRNA/R-gene interactions acting as a possible source of functional diploidization of structurally retained R-genes duplicates. Such evolutionary shuffling events leaded to CNVs (i.e. Copy Number Variation) and PAVs (i.e. Presence Absence Variation) between related species operating in the decay of R-genes colinearity between plant species.

【 授权许可】

   
2014 Zhang et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 1.

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【 参考文献 】

• [1]Glazebrook J: Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 2005, 43:205-227.
• [2]Pallas V, Garcia JA: How do plant viruses induce disease? Interactions and interference with host components. J Gen Virol 2011, 92(Pt 12):2691-2705.
• [3]Soriano IR, Riley IT, Potter MJ, Bowers WS: Phytoecdysteroids: a novel defense against plant-parasitic nematodes. J Chem Ecol 2004, 30(10):1885-1899.
• [4]Choy A, Roy CR: Autophagy and bacterial infection: an evolving arms race. Trends Microbiol 2013, 21(9):451-456.
• [5]Chisholm ST, Coaker G, Day B, Staskawicz BJ: Host-microbe interactions: shaping the evolution of the plant immune response. Cell 2006, 124(4):803-814.
• [6]Medzhitov R, Janeway CA Jr: Innate immunity: the virtues of a nonclonal system of recognition. Cell 1997, 91(3):295-298.
• [7]Nurnberger T, Brunner F: Innate immunity in plants and animals: emerging parallels between the recognition of general elicitors and pathogen-associated molecular patterns. Curr Opin Plant Biol 2002, 5(4):318-324.
• [8]Mur LAJ, Kenton P, Lloyd AJ, Ougham H, Prats E: The hypersensitive response; the centenary is upon us but how much do we know? J Exp Bot 2008, 59(3):20.
• [9]Hammond-Kosack KE, Parker JE: Deciphering plant-pathogen communication: fresh perspectives for molecular resistance breeding. Curr Opin Biotechnol 2003, 14(2):177-193.
• [10]Glowacki S, Macioszek VK, Kononowicz AK: R proteins as fundamentals of plant innate immunity. Cell Mol Biol Lett 2011, 16(1):1-24.
• [11]Qiu D, Xiao J, Ding X, Xiong M, Cai M, Cao Y, Li X, Xu C, Wang S: OsWRKY13 mediates rice disease resistance by regulating defense-related genes in salicylate- and jasmonate-dependent signaling. Mol Plant Microbe Interact 2007, 20(5):492-499.
• [12]Shimono M, Koga H, Akagi A, Hayashi N, Goto S, Sawada M, Kurihara T, Matsushita A, Sugano S, Jiang CJ, Kaku H, Inoue H, Takatsuji H: Rice WRKY45 plays important roles in fungal and bacterial disease resistance. Mol Plant Pathol 2012, 13(1):83-94.
• [13]Spaink HP: Specific recognition of bacteria by plant LysM domain receptor kinases. Trends Microbiol 2004, 12(5):201-204.
• [14]Buist G, Steen A, Kok J, Kuipers OP: LysM, a widely distributed protein motif for binding to (peptido)glycans. Mol Microbiol 2008, 68(4):838-847.
• [15]Witte CP, Keinath N, Dubiella U, Demouliere R, Seal A, Romeis T: Tobacco calcium-dependent protein kinases are differentially phosphorylated in vivo as part of a kinase cascade that regulates stress response. J Biol Chem 2010, 285(13):9740-9748.
• [16]Kurusu T, Hamada J, Nokajima H, Kitagawa Y, Kiyoduka M, Takahashi A, Hanamata S, Ohno R, Hayashi T, Okada K, Koga J, Hirochika H, Yamane H, Kuchitsu K: Regulation of microbe-associated molecular pattern-induced hypersensitive cell death, phytoalexin production, and defense gene expression by calcineurin B-like protein-interacting protein kinases, OsCIPK14/15, in rice cultured cells. Plant Physiol 2010, 153(2):678-692.
• [17]Bent AF: Plant disease resistance genes: function meets structure. Plant Cell 1996, 8(10):1757-1771.
• [18]Wang J, Tan S, Zhang L, Li P, Tian D: Co-variation among major classes of LRR-encoding genes in two pairs of plant species. J Mol Evol 2011, 72(5–6):498-509.
• [19]Panstruga R, Parker JE, Schulze-Lefert P: SnapShot: plant immune response pathways. Cell 2009, 136(5):978. e971-973
• [20]Yue JX, Meyers BC, Chen JQ, Tian D, Yang S: Tracing the origin and evolutionary history of plant nucleotide-binding site-leucine-rich repeat (NBS-LRR) genes. New Phytol 2012, 193(4):1049-1063.
• [21]Meyers BC, Dickerman AW, Michelmore RW, Sivaramakrishnan S, Sobral BW, Young ND: Plant disease resistance genes encode members of an ancient and diverse protein family within the nucleotide-binding superfamily. Plant J 1999, 20(3):317-332.
• [22]Akita M, Valkonen JP: A novel gene family in moss (Physcomitrella patens) shows sequence homology and a phylogenetic relationship with the TIR-NBS class of plant disease resistance genes. J Mol Evol 2002, 55(5):595-605.
• [23]Bertin J, Nir WJ, Fischer CM, Tayber OV, Errada PR, Grant JR, Keilty JJ, Gosselin ML, Robison KE, Wong GH, Glucksmann MA, DiStefano PS: Human CARD4 protein is a novel CED-4/Apaf-1 cell death family member that activates NF-kappaB. J Biol Chem 1999, 274(19):12955-12958.
• [24]Meyers BC, Morgante M, Michelmore RW: TIR-X and TIR-NBS proteins: two new families related to disease resistance TIR-NBS-LRR proteins encoded in Arabidopsis and other plant genomes. Plant J 2002, 32(1):77-92.
• [25]Liu JJ, Ekramoddoullah AK: Isolation, genetic variation and expression of TIR-NBS-LRR resistance gene analogs from western white pine ( Pinus monticola Dougl. ex. D. Don). Mol Genet Genomics 2003, 270(5):432-441.
• [26]Girardin SE, Sansonetti PJ, Philpott DJ: Intracellular vs extracellular recognition of pathogens–common concepts in mammals and flies. Trends Microbiol 2002, 10(4):193-199.
• [27]Tarr DE, Alexander HM: TIR-NBS-LRR genes are rare in monocots: evidence from diverse monocot orders. BMC Res Notes 2009, 2:197. BioMed Central Full Text
• [28]Bai J, Pennill LA, Ning J, Lee SW, Ramalingam J, Webb CA, Zhao B, Sun Q, Nelson JC, Leach JE, Hulbert SH: Diversity in nucleotide binding site-leucine-rich repeat genes in cereals. Genome Res 2002, 12(12):1871-1884.
• [29]Meyers BC, Kozik A, Griego A, Kuang H, Michelmore RW: Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 2003, 15(4):809-834.
• [30]Yang S, Zhang X, Yue JX, Tian D, Chen JQ: Recent duplications dominate NBS-encoding gene expansion in two woody species. Mol Genet Genomics 2008, 280(3):187-198.
• [31]Porter BW, Paidi M, Ming R, Alam M, Nishijima WT, Zhu YJ: Genome-wide analysis of Carica papaya reveals a small NBS resistance gene family. Mol Genet Genomics 2009, 281(6):609-626.
• [32]Leister D: Tandem and segmental gene duplication and recombination in the evolution of plant disease resistance gene. Trends Genet 2004, 20(3):116-122.
• [33]Luo S, Zhang Y, Hu Q, Chen J, Li K, Lu C, Liu H, Wang W, Kuang H: Dynamic nucleotide-binding site and leucine-rich repeat-encoding genes in the grass family. Plant Physiol 2012, 159(1):197-210.
• [34]Guo YL, Fitz J, Schneeberger K, Ossowski S, Cao J, Weigel D: Genome-wide comparison of nucleotide-binding site-leucine-rich repeat-encoding genes in Arabidopsis. Plant Physiol 2011, 157(2):757-769.
• [35]Shen J, Araki H, Chen L, Chen JQ, Tian D: Unique evolutionary mechanism in R-genes under the presence/absence polymorphism in Arabidopsis thaliana. Genetics 2006, 172(2):1243-1250.
• [36]Yang S, Feng Z, Zhang X, Jiang K, Jin X, Hang Y, Chen JQ, Tian D: Genome-wide investigation on the genetic variations of rice disease resistance genes. Plant Mol Biol 2006, 62(1–2):181-193.
• [37]Leister D, Kurth J, Laurie DA, Yano M, Sasaki T, Devos K, Graner A, Schulze-Lefert P: Rapid reorganization of resistance gene homologues in cereal genomes. Proc Natl Acad Sci U S A 1998, 95(1):370-375.
• [38]Meyers BC, Kaushik S, Nandety RS: Evolving disease resistance genes. Curr Opin Plant Biol 2005, 8(2):129-134.
• [39]Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A, Schmutz J, Spannagl M, Tang H, Wang X, Wicker T, Bharti AK, Chapman J, Feltus FA, Gowik U, Grigoriev IV, Lyons E, Maher CA, Martis M, Narechania A, Otillar RP, Penning BW, Salamov AA, Wang Y, Zhang L, Carpita NC, et al.: The Sorghum bicolor genome and the diversification of grasses. Nature 2009, 457(7229):551-556.
• [40]Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, Liang C, Zhang J, Fulton L, Graves TA, Minx P, Reily AD, Courtney L, Kruchowski SS, Tomlinson C, Strong C, Delehaunty K, Fronick C, Courtney B, Rock SM, Belter E, Du F, Kim K, Abbott RM, Cotton M, Levy A, Marchetto P, Ochoa K, Jackson SM, Gillam B, et al.: The B73 maize genome: complexity, diversity, and dynamics. Science 2009, 326(5956):1112-1115.
• [41]International Rice Genome Sequencing P: The map-based sequence of the rice genome. Nature 2005, 436(7052):793-800.
• [42]International Brachypodium I: Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature 2010, 463(7282):763-768.
• [43]Salse J, Abrouk M, Bolot S, Guilhot N, Courcelle E, Faraut T, Waugh R, Close TJ, Messing J, Feuillet C: Reconstruction of monocotelydoneous proto-chromosomes reveals faster evolution in plants than in animals. Proc Natl Acad Sci U S A 2009, 106(35):14908-14913.
• [44]Salse J, Abrouk M, Murat F, Quraishi UM, Feuillet C: Improved criteria and comparative genomics tool provide new insights into grass paleogenomics. Brief Bioinform 2009, 10(6):619-630.
• [45]Bolot S, Abrouk M, Masood-Quraishi U, Stein N, Messing J, Feuillet C, Salse J: The ‘inner circle’ of the cereal genomes. Curr Opin Plant Biol 2009, 12(2):119-125.
• [46]Jaillon O, Aury JM, Noel B, Policriti A, Clepet C, Casagrande A, Choisne N, Aubourg S, Vitulo N, Jubin C, Vezzi A, Legeai F, Hugueney P, Dasilva C, Horner D, Mica E, Jublot D, Poulain J, Bruyère C, Billault A, Segurens B, Gouyvenoux M, Ugarte E, Cattonaro F, Anthouard V, Vico V, Del Fabbro C, Alaux M, Di Gaspero G, Dumas V, et al.: The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 2007, 449(7161):463-467.
• [47]Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, Schein J, Sterck L, Aerts A, Bhalerao RR, Bhalerao RP, Blaudez D, Boerjan W, Brun A, Brunner A, Busov V, Campbell M, Carlson J, Chalot M, Chapman J, Chen GL, Cooper D, Coutinho PM, Couturier J, Covert S, Cronk Q, et al.: The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 2006, 313(5793):1596-1604.
• [48]Arabidopsis Genome I: Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 2000, 408(6814):796-815.
• [49]Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, Xu D, Hellsten U, May GD, Yu Y, Sakurai T, Umezawa T, Bhattacharyya MK, Sandhu D, Valliyodan B, Lindquist E, Peto M, Grant D, Shu S, Goodstein D, Barry K, Futrell-Griggs M, Abernathy B, Du J, Tian Z, Zhu L, et al.: Genome sequence of the palaeopolyploid soybean. Nature 2010, 463(7278):178-183.
• [50]Argout X, Salse J, Aury JM, Guiltinan MJ, Droc G, Gouzy J, Allegre M, Chaparro C, Legavre T, Maximova SN, Abrouk M, Murat F, Fouet O, Poulain J, Ruiz M, Roguet Y, Rodier-Goud M, Barbosa-Neto JF, Sabot F, Kudrna D, Ammiraju JS, Schuster SC, Carlson JE, Sallet E, Schiex T, Dievart A, Kramer M, Gelley L, Shi Z, Bérard A, et al.: The genome of Theobroma cacao. Nat Genet 2011, 43(2):101-108.
• [51]Abrouk M, Murat F, Pont C, Messing J, Jackson S, Faraut T, Tannier E, Plomion C, Cooke R, Feuillet C, Salse J: Palaeogenomics of plants: synteny-based modelling of extinct ancestors. Trends Plant Sci 2010, 15(9):479-487.
• [52]Paterson AH, Bowers JE, Chapman BA: Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics. Proc Natl Acad Sci U S A 2004, 101(26):9903-9908.
• [53]Tang H, Bowers JE, Wang X, Ming R, Alam M, Paterson AH: Synteny and collinearity in plant genomes. Science 2008, 320(5875):486-488.
• [54]Tang H, Wang X, Bowers JE, Ming R, Alam M, Paterson AH: Unraveling ancient hexaploidy through multiply-aligned angiosperm gene maps. Genome Res 2008, 18(12):1944-1954.
• [55]Van de Peer Y, Fawcett JA, Proost S, Sterck L, Vandepoele K: The flowering world: a tale of duplications. Trends Plant Sci 2009, 14(12):680-688.
• [56]Bowers JE, Chapman BA, Rong J, Paterson AH: Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 2003, 422(6930):433-438.
• [57]Lawton-Rauh A: Evolutionary dynamics of duplicated genes in plants. Mol Phylogenet Evol 2003, 29(3):396-409.
• [58]Blanc G, Wolfe KH: Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes. Plant Cell 2004, 16(7):1667-1678.
• [59]Velasco R, Zharkikh A, Troggio M, Cartwright DA, Cestaro A, Pruss D, Pindo M, Fitzgerald LM, Vezzulli S, Reid J, Malacarne G, Iliev D, Coppola G, Wardell B, Micheletti D, Macalma T, Facci M, Mitchell JT, Perazzolli M, Eldredge G, Gatto P, Oyzerski R, Moretto M, Gutin N, Stefanini M, Chen Y, Segala C, Davenport C, Demattè L, Mraz A, et al.: A high quality draft consensus sequence of the genome of a heterozygous grapevine variety. PLoS One 2007, 2(12):e1326.
• [60]Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A, Fontana P, Bhatnagar SK, Troggio M, Pruss D, Salvi S, Pindo M, Baldi P, Castelletti S, Cavaiuolo M, Coppola G, Costa F, Cova V, Dal Ri A, Goremykin V, Komjanc M, Longhi S, Magnago P, Malacarne G, Malnoy M, Micheletti D, Moretto M, Perazzolli M, Si-Ammour A, Vezzulli S, et al.: The genome of the domesticated apple (Malus x domestica Borkh). Nat Genet 2010, 42(10):833-839.
• [61]Sato S, Nakamura Y, Kaneko T, Asamizu E, Kato T, Nakao M, Sasamoto S, Watanabe A, Ono A, Kawashima K, Fujishiro T, Katoh M, Kohara M, Kishida Y, Minami C, Nakayama S, Nakazaki N, Shimizu Y, Shinpo S, Takahashi C, Wada T, Yamada M, Ohmido N, Hayashi M, Fukui K, Baba T, Nakamichi T, Mori H, Tabata S: Genome structure of the legume, Lotus japonicus. DNA Res 2008, 15(4):227-239.
• [62]Shulaev V, Sargent DJ, Crowhurst RN, Mockler TC, Folkerts O, Delcher AL, Jaiswal P, Mockaitis K, Liston A, Mane SP, Burns P, Davis TM, Slovin JP, Bassil N, Hellens RP, Evans C, Harkins T, Kodira C, Desany B, Crasta OR, Jensen RV, Allan AC, Michael TP, Setubal JC, Celton JM, Rees DJ, Williams KP, Holt SH, Ruiz Rojas JJ, Chatterjee M, et al.: The genome of woodland strawberry (Fragaria vesca). Nat Genet 2011, 43(2):109-116.
• [63]Ming R, Hou S, Feng Y, Yu Q, Dionne-Laporte A, Saw JH, Senin P, Wang W, Ly BV, Lewis KL, Salzberg SL, Feng L, Jones MR, Skelton RL, Murray JE, Chen C, Qian W, Shen J, Du P, Eustice M, Tong E, Tang H, Lyons E, Paull RE, Michael TP, Wall K, Rice DW, Albert H, Wang ML, Zhu YJ: The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus). Nature 2008, 452(7190):991-996.
• [64]Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, Sonnhammer EL, Tate J, Punta M: The Pfam protein families database. Nucleic Acids Res 2014, 42(Database issue):D222-D230.
• [65]Sanseverino W, Roma G, De Simone M, Faino L, Melito S, Stupka E, Frusciante L, Ercolano MR: PRGdb: a bioinformatics platform for plant resistance gene analysis. Nucleic Acids Res 2010, 38(Database issue):D814-D821.
• [66]Salse J: In silico archeogenomics unveils modern plant genome organisation, regulation and evolution. Curr Opin Plant Biol 2012, 15(2):122-130.
• [67]Murat F, Xu JH, Tannier E, Abrouk M, Guilhot N, Pont C, Messing J, Salse J: Ancestral grass karyotype reconstruction unravels new mechanisms of genome shuffling as a source of plant evolution. Genome Res 2010, 20(11):1545-1557.
• [68]Abrouk M, Zhang R, Murat F, Li A, Pont C, Mao L, Salse J: Grass microRNA gene paleohistory unveils new insights into gene dosage balance in subgenome partitioning after whole-genome duplication. Plant Cell 2012, 24(5):1776-1792.
• [69]Schnable JC, Freeling M, Lyons E: Genome-wide analysis of syntenic gene deletion in the grasses. Genome Biol Evol 2012, 4(3):265-277.
• [70]Thomas BC, Pedersen B, Freeling M: Following tetraploidy in an Arabidopsis ancestor, genes were removed preferentially from one homeolog leaving clusters enriched in dose-sensitive genes. Genome Res 2006, 16(7):934-946.
• [71]Sankoff D, Zheng C, Zhu Q: The collapse of gene complement following whole genome duplication. BMC Genomics 2010, 11:313. BioMed Central Full Text
• [72]Xiong Y, Liu T, Tian C, Sun S, Li J, Chen M: Transcription factors in rice: a genome-wide comparative analysis between monocots and eudicots. Plant Mol Biol 2005, 59(1):191-203.
• [73]Freeling M: Bias in plant gene content following different sorts of duplication: tandem, whole-genome, segmental, or by transposition. Annu Rev Plant Biol 2009, 60:433-453.
• [74]Richly E, Kurth J, Leister D: Mode of amplification and reorganization of resistance genes during recent Arabidopsis thaliana evolution. Mol Biol Evol 2002, 19(1):76-84.
• [75]Xu Z, Wang H: LTR_FINDER: an efficient tool for the prediction of full-length LTR retrotransposons. Nucleic Acids Res 2007, 35(Web Server issue):W265-W268.
• [76]Wicker T, Buchmann JP, Keller B: Patching gaps in plant genomes results in gene movement and erosion of colinearity. Genome Res 2010, 20(9):1229-1237.
• [77]Reinhart BJ, Weinstein EG, Rhoades MW, Bartel B, Bartel DP: MicroRNAs in plants. Genes Dev 2002, 16(13):1616-1626.
• [78]Lim LP, Glasner ME, Yekta S, Burge CB, Bartel DP: Vertebrate microRNA genes. Science 2003, 299(5612):1540.
• [79]Bagga S, Pasquinelli AE: Identification and analysis of microRNAs. Genet Eng 2006, 27:1-20.
• [80]Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, Voinnet O, Jones JD: A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 2006, 312(5772):436-439.
• [81]Li Y, Zhang Q, Zhang J, Wu L, Qi Y, Zhou JM: Identification of microRNAs involved in pathogen-associated molecular pattern-triggered plant innate immunity. Plant Physiol 2010, 152(4):2222-2231.
• [82]Du P, Wu J, Zhang J, Zhao S, Zheng H, Gao G, Wei L, Li Y: Viral infection induces expression of novel phased microRNAs from conserved cellular microRNA precursors. PLoS Pathog 2011, 7(8):e1002176.
• [83]Katiyar-Agarwal S, Morgan R, Dahlbeck D, Borsani O, Villegas A Jr, Zhu JK, Staskawicz BJ, Jin H: A pathogen-inducible endogenous siRNA in plant immunity. Proc Natl Acad Sci U S A 2006, 103(47):18002-18007.
• [84]Allen E, Xie Z, Gustafson AM, Carrington JC: microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 2005, 121(2):207-221.
• [85]McHale LK, Haun WJ, Xu WW, Bhaskar PB, Anderson JE, Hyten DL, Gerhardt DJ, Jeddeloh JA, Stupar RM: Structural variants in the soybean genome localize to clusters of biotic stress-response genes. Plant Physiol 2012, 159(4):1295-1308.
• [86]Chantret N, Salse J, Sabot F, Rahman S, Bellec A, Laubin B, Dubois I, Dossat C, Sourdille P, Joudrier P, Gautier MF, Cattolico L, Beckert M, Aubourg S, Weissenbach J, Caboche M, Bernard M, Leroy P, Chalhoub B: Molecular basis of evolutionary events that shaped the hardness locus in diploid and polyploid wheat species (Triticum and Aegilops). Plant Cell 2005, 17(4):1033-1045.
• [87]Sun X, Wang GL: Genome-wide identification, characterization and phylogenetic analysis of the rice LRR-kinases. PLoS One 2011, 6(3):e16079.
• [88]Zhai J, Jeong DH, De Paoli E, Park S, Rosen BD, Li Y, González AJ, Yan Z, Kitto SL, Grusak MA, Jackson SA, Stacey G, Cook DR, Green PJ, Sherrier DJ, Meyers BC: MicroRNAs as master regulators of the plant NB-LRR defense gene family via the production of phased, trans-acting siRNAs. Genes Dev 2011, 25(23):2540-2553.
• [89]Li F, Pignatta D, Bendix C, Brunkard JO, Cohn MM, Tung J, Sun H, Kumar P, Baker B: MicroRNA regulation of plant innate immune receptors. Proc Natl Acad Sci U S A 2012, 109(5):1790-1795.
• [90]Eckardt NA: A microRNA cascade in plant defense. Plant Cell 2012, 24(3):840.
• [91]Finn RD, Clements J, Eddy SR: HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 2011, 39(Web Server issue):W29-W37.
• [92]Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA: Circos: an information aesthetic for comparative genomics. Genome Res 2009, 19(9):1639-1645.
• [93]Mathelier A, Carbone A: MIReNA: finding microRNAs with high accuracy and no learning at genome scale and from deep sequencing data. Bioinformatics 2010, 26(18):2226-2234.