The DOI matches its Crossref record; 159 of the 159 references it cites were found in a registry or an index.
Origin and evolution of the plant immune system
Open accessAbstract
ContentsSummary70I.Introduction70II.Ancient associations between plants and microbes72III.Evolutionary dynamics of plant–pathogen interactions74IV.Evolutionary signature of plant–pathogen interactions74V.Origin and evolution of RLK proteins75VI.Origin and evolution of NLR proteins77VII.Origin and evolution of SA signaling78VIII.Origin and evolution of RNA‐based defense79IX.Perspectives79Acknowledgements80References80 Summary: Microbes have engaged in antagonistic associations with plants for hundreds of millions of years. Plants, in turn, have evolved diverse immune strategies to combat microbial pathogens. The conflicts between plants and pathogens result in everchanging coevolutionary cycles known as ‘Red Queen’ dynamics. These ancient and ongoing plant–pathogen interactions have shaped the evolution of both plant and pathogen genomes. With the recent explosion of plant genome‐scale data, comparative analyses provide novel insights into the coevolutionary dynamics of plants and pathogens. Here, we discuss the ancient associations between plants and microbes as well as the evolutionary principles underlying plant–pathogen interactions. We synthesize and review the current knowledge on the origin and evolution of key components of the plant immune system. We also highlight the importance of studying algae and nonflowering land plants in understanding the evolution of the plant immune system.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Statistical method for testing the neutral mutation hypothesis by DNA polymorphism.
Tajima, F. (1989) · Genetics · doi:10.1093/genetics/123.3.585 · Cited by 13,941
Jones, J. D. G., & Dangl, J. L. (2006) · Nature · doi:10.1038/nature05286 · Cited by 13,177
The Evolutionary Fate and Consequences of Duplicate Genes
Lynch, M., & Conery, J. S. (2000) · Science · doi:10.1126/science.290.5494.1151 · Cited by 4,988
Hanski, L. (1999) · doi:10.1093/oso/9780198540663.001.0001 · Cited by 3,535
Some Demographic and Genetic Consequences of Environmental Heterogeneity for Biological Control
Levins, R. (1969) · Bulletin of the Entomological Society of America · doi:10.1093/besa/15.3.237 · Cited by 3,474
Boller, T., & Felix, G. (2009) · Annual Review of Plant Biology · doi:10.1146/annurev.arplant.57.032905.105346 · Cited by 3,387
Structure and functions of the bacterial microbiota of plants
Bulgarelli, D., Schlaeppi, K., Spaepen, S., van Themaat, E. V. L., & Schulze-Lefert, P. (2013) · Annual Review of Plant Biology · doi:10.1146/annurev-arplant-050312-120106 · Cited by 3,308
TimeTree: A Resource for Timelines, Timetrees, and Divergence Times
Kumar, S., Stecher, G., Suleski, M., & Hedges, S. B. (2017) · Molecular Biology and Evolution · doi:10.1093/molbev/msx116 · Cited by 2,721
Valen, L. M. V. (1973) · Medical Entomology and Zoology · Cited by 2,448
The Geographic Mosaic of Coevolution
Thompson, J. N. (2005) · doi:10.7208/chicago/9780226118697.001.0001 · Cited by 2,083
Molecular evidence for glacial refugia of mountain plants in the European Alps
SCHÖNSWETTER, P., STEHLIK, I., HOLDEREGGER, R., & TRIBSCH, A. (2005) · Molecular Ecology · doi:10.1111/j.1365-294x.2005.02683.x · Cited by 2,067
Reconstructing the early evolution of Fungi using a six-gene phylogeny
James, T. Y., Kauff, F., Schoch, C. L., Matheny, P. B., Hofstetter, V., Cox, C. J., Celio, G., Gueidan, C., Fraker, E., Miadlikowska, J., et al. (2006) · Nature · doi:10.1038/nature05110 · Cited by 1,815
Detecting Individual Sites Subject to Episodic Diversifying Selection
Murrell, B., Wertheim, J. O., Moola, S., Weighill, T., Scheffler, K., & Kosakovsky Pond, S. L. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1002764 · Cited by 1,811
Statistical methods for detecting molecular adaptation
Yang, Z., & Bielawski, J. P. (2000) · Trends in Ecology & Evolution · doi:10.1016/s0169-5347(00)01994-7 · Cited by 1,806
A Test of Neutral Molecular Evolution Based on Nucleotide Data
Hudson, R. R., Kreitman, M., & Aguadé, M. (1987) · Genetics · doi:10.1093/genetics/116.1.153 · Cited by 1,767
Molecular Signatures of Natural Selection
Nielsen, R. (2005) · Annual Review of Genetics · doi:10.1146/annurev.genet.39.073003.112420 · Cited by 1,641
Genome-Wide Analysis of NBS-LRR–Encoding Genes in Arabidopsis[W]
Meyers, B. C., Kozik, A., Griego, A., Kuang, H., & Michelmore, R. W. (2003) · The Plant Cell · doi:10.1105/tpc.009308 · Cited by 1,605
The geographic mosaic of coevolution
(2005) · Choice Reviews Online · doi:10.5860/choice.43-2194 · Cited by 1,586
Systemic Acquired Resistance: Turning Local Infection into Global Defense
Fu, Z. Q., & Dong, X. (2013) · Annual Review of Plant Biology · doi:10.1146/annurev-arplant-042811-105606 · Cited by 1,524
Shiu, S.-H., & Bleecker, A. B. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.181141598 · Cited by 1,495
Regulation of pattern recognition receptor signalling in plants
Couto, D., & Zipfel, C. (2016) · Nature Reviews Immunology · doi:10.1038/nri.2016.77 · Cited by 1,393
Phylotranscriptomic analysis of the origin and early diversification of land plants
Wickett, N. J., Mirarab, S., Nguyen, N., Warnow, T., Carpenter, E., Matasci, N., Ayyampalayam, S., Barker, M. S., Burleigh, J. G., Gitzendanner, M. A., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1323926111 · Cited by 1,252
Insights into Land Plant Evolution Garnered from the Marchantia polymorpha Genome
Bowman, J. L., Kohchi, T., Yamato, K. T., Jenkins, J., Shu, S., Ishizaki, K., Yamaoka, S., Nishihama, R., Nakamura, Y., Berger, F., et al. (2017) · Cell · doi:10.1016/j.cell.2017.09.030 · Cited by 1,205
Plant pattern-recognition receptors
Zipfel, C. (2014) · Trends in Immunology · doi:10.1016/j.it.2014.05.004 · Cited by 1,159
Comparative Analysis of the Receptor-Like Kinase Family in Arabidopsis and Rice[W]
Shiu, S.-H., Karlowski, W. M., Pan, R., Tzeng, Y.-H., Mayer, K. F. X., & Li, W.-H. (2004) · The Plant Cell · doi:10.1105/tpc.020834 · Cited by 1,139
Phylogeographic studies in plants: problems and prospects
SCHAAL, B. A., HAYWORTH, D. A., OLSEN, K. M., RAUSCHER, J. T., & SMITH, W. A. (1998) · Molecular Ecology · doi:10.1046/j.1365-294x.1998.00318.x · Cited by 1,123
How do plants achieve immunity? Defence without specialized immune cells
Spoel, S. H., & Dong, X. (2012) · Nature Reviews Immunology · doi:10.1038/nri3141 · Cited by 1,112
Of PAMPs and Effectors: The Blurred PTI-ETI Dichotomy
Thomma, B. P. H. J., Nürnberger, T., & Joosten, M. H. A. J. (2011) · The Plant Cell · doi:10.1105/tpc.110.082602 · Cited by 1,064
Molecular Evidence for the Early Colonization of Land by Fungi and Plants
Heckman, D. S., Geiser, D. M., Eidell, B. R., Stauffer, R. L., Kardos, N. L., & Hedges, S. B. (2001) · Science · doi:10.1126/science.1061457 · Cited by 1,020
Plant NBS-LRR proteins: adaptable guards.
McHale, L. K., Tan, X., Koehl, P., & Michelmore, R. W. (2006) · Genome biology · doi:10.1186/gb-2006-7-4-212 · Cited by 1,008
Are innate immune signaling pathways in plants and animals conserved?
Ausubel, F. M. (2005) · Nature Immunology · doi:10.1038/ni1253 · Cited by 976
The N Terminus of Bacterial Elongation Factor Tu Elicits Innate Immunity in Arabidopsis Plants
Kunze, G., Zipfel, C., Robatzek, S., Niehaus, K., Boller, T., & Felix, G. (2004) · The Plant Cell · doi:10.1105/tpc.104.026765 · Cited by 954
Expansion of the Receptor-Like Kinase/Pelle Gene Family and Receptor-Like Proteins in Arabidopsis
Shiu, S.-H., & Bleecker, A. B. (2003) · Plant Physiology · doi:10.1104/pp.103.021964 · Cited by 933
Chinchilla, D., Bauer, Z., Regenass, M., Boller, T., & Felix, G. (2006) · The Plant Cell · doi:10.1105/tpc.105.036574 · Cited by 922
Estimating the timing of early eukaryotic diversification with multigene molecular clocks
Parfrey, L. W., Lahr, D. J. G., Knoll, A. H., & Katz, L. A. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1110633108 · Cited by 899
Phylogeny and Molecular Evolution of the Green Algae
Leliaert, F., Smith, D. R., Moreau, H., Herron, M. D., Verbruggen, H., Delwiche, C. F., & De Clerck, O. (2012) · Critical Reviews in Plant Sciences · doi:10.1080/07352689.2011.615705 · Cited by 896
Receptor Kinases in Plant-Pathogen Interactions: More Than Pattern Recognition
Tang, D., Wang, G., & Zhou, J.-M. (2017) · The Plant Cell · doi:10.1105/tpc.16.00891 · Cited by 877
Biological and biomedical implications of the co-evolution of pathogens and their hosts
Woolhouse, M. E. J., Webster, J. P., Domingo, E., Charlesworth, B., & Levin, B. R. (2002) · Nature Genetics · doi:10.1038/ng1202-569 · Cited by 869
Ding, S.-W. (2010) · Nature Reviews Immunology · doi:10.1038/nri2824 · Cited by 860
Plant signalling in symbiosis and immunity
Zipfel, C., & Oldroyd, G. E. D. (2017) · Nature · doi:10.1038/nature22009 · Cited by 843
Kourelis, J., & van der Hoorn, R. A. L. (2018) · The Plant Cell · doi:10.1105/tpc.17.00579 · Cited by 791
Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana
Tian, D., Traw, M. B., Chen, J. Q., Kreitman, M., & Bergelson, J. (2003) · Nature · doi:10.1038/nature01588 · Cited by 788
From Guard to Decoy: A New Model for Perception of Plant Pathogen Effectors
van der Hoorn, R. A. L., & Kamoun, S. (2008) · The Plant Cell · doi:10.1105/tpc.108.060194 · Cited by 784
Ding, Y., Sun, T., Ao, K., Peng, Y., Zhang, Y., Li, X., & Zhang, Y. (2018) · Cell · doi:10.1016/j.cell.2018.03.044 · Cited by 739
A MicroRNA Superfamily Regulates Nucleotide Binding Site–Leucine-Rich Repeats and Other mRNAs
Shivaprasad, P. V., Chen, H.-M., Patel, K., Bond, D. M., Santos, B. A. C. M., & Baulcombe, D. C. (2012) · The Plant Cell · doi:10.1105/tpc.111.095380 · Cited by 728
Dimensions of biodiversity in the Earth mycobiome
Peay, K. G., Kennedy, P. G., & Talbot, J. M. (2016) · Nature Reviews Microbiology · doi:10.1038/nrmicro.2016.59 · Cited by 721
Balancing Selection and Its Effects on Sequences in Nearby Genome Regions
Charlesworth, D. (2006) · PLoS Genetics · doi:10.1371/journal.pgen.0020064 · Cited by 717
Detecting Natural Selection in Genomic Data
Vitti, J. J., Grossman, S. R., & Sabeti, P. C. (2013) · Annual Review of Genetics · doi:10.1146/annurev-genet-111212-133526 · Cited by 694
High-level classification of the Fungi and a tool for evolutionary ecological analyses
Tedersoo, L., Sánchez-Ramírez, S., Kõljalg, U., Bahram, M., Döring, M., Schigel, D., May, T., Ryberg, M., & Abarenkov, K. (2018) · Fungal Diversity · doi:10.1007/s13225-018-0401-0 · Cited by 693
Reading the entrails of chickens: molecular timescales of evolution and the illusion of precision
Graur, D., & Martin, W. (2004) · Trends in Genetics · doi:10.1016/j.tig.2003.12.003 · Cited by 669
Multiple reference genomes and transcriptomes for Arabidopsis thaliana
Gan, X., Stegle, O., Behr, J., Steffen, J. G., Drewe, P., Hildebrand, K. L., Lyngsoe, R., Schultheiss, S. J., Osborne, E. J., Sreedharan, V. T., et al. (2011) · Nature · doi:10.1038/nature10414 · Cited by 643
RNA silencing suppression by plant pathogens: defence, counter-defence and counter-counter-defence
Pumplin, N., & Voinnet, O. (2013) · Nature Reviews Microbiology · doi:10.1038/nrmicro3120 · Cited by 642
Gould, S. B., Waller, R. F., & McFadden, G. I. (2008) · Annual Review of Plant Biology · doi:10.1146/annurev.arplant.59.032607.092915 · Cited by 634
From Chaos to Harmony: Responses and Signaling upon Microbial Pattern Recognition
Yu, X., Feng, B., He, P., & Shan, L. (2017) · Annual Review of Phytopathology · doi:10.1146/annurev-phyto-080516-035649 · Cited by 604
Population genetics: a concise guide
(1998) · Choice Reviews Online · doi:10.5860/choice.35-4473 · Cited by 601
Dynamics of disease resistance polymorphism at the Rpm1 locus of Arabidopsis
Stahl, E. A., Dwyer, G., Mauricio, R., Kreitman, M., & Bergelson, J. (1999) · Nature · doi:10.1038/23260 · Cited by 600
Microbial Biogeography: From Taxonomy to Traits
Green, J. L., Bohannan, B. J. M., & Whitaker, R. J. (2008) · Science · doi:10.1126/science.1153475 · Cited by 594
Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation
Hori, K., Maruyama, F., Fujisawa, T., Togashi, T., Yamamoto, N., Seo, M., Sato, S., Yamada, T., Mori, H., Tajima, N., et al. (2014) · Nature Communications · doi:10.1038/ncomms4978 · Cited by 588
A Plant Immune Receptor Detects Pathogen Effectors that Target WRKY Transcription Factors
Sarris, P. F., Duxbury, Z., Huh, S. U., Ma, Y., Segonzac, C., Sklenar, J., Derbyshire, P., Cevik, V., Rallapalli, G., Saucet, S. B., et al. (2015) · Cell · doi:10.1016/j.cell.2015.04.024 · Cited by 565
Origins and evolution of eukaryotic RNA interference
SHABALINA, S., & KOONIN, E. (2008) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2008.06.005 · Cited by 561
The Chara Genome: Secondary Complexity and Implications for Plant Terrestrialization
Nishiyama, T., Sakayama, H., de Vries, J., Buschmann, H., Saint-Marcoux, D., Ullrich, K. K., Haas, F. B., Vanderstraeten, L., Becker, D., Lang, D., et al. (2018) · Cell · doi:10.1016/j.cell.2018.06.033 · Cited by 525
Rules of engagement: molecular insights from host–virus arms races
Daugherty, M. D., & Malik, H. S. (2012) · Annual Review of Genetics · doi:10.1146/annurev-genet-110711-155522 · Cited by 515
Evolutionary Dynamics of Plant R -Genes
Bergelson, J., Kreitman, M., Stahl, E. A., & Tian, D. (2001) · Science · doi:10.1126/science.1061337 · Cited by 510
Cladosporium Avr2 Inhibits Tomato Rcr3 Protease Required for Cf-2 -Dependent Disease Resistance
Rooney, H. C. E., van't Klooster, J. W., van der Hoorn, R. A. L., Joosten, M. H. A. J., Jones, J. D. G., & de Wit, P. J. G. M. (2005) · Science · doi:10.1126/science.1111404 · Cited by 501
The Interrelationships of Land Plants and the Nature of the Ancestral Embryophyte
Puttick, M. N., Morris, J. L., Williams, T. A., Cox, C. J., Edwards, D., Kenrick, P., Pressel, S., Wellman, C. H., Schneider, H., Pisani, D., et al. (2018) · Current Biology · doi:10.1016/j.cub.2018.01.063 · Cited by 498
Le Roux, C., Huet, G., Jauneau, A., Camborde, L., Trémousaygue, D., Kraut, A., Zhou, B., Levaillant, M., Adachi, H., Yoshioka, H., et al. (2015) · Cell · doi:10.1016/j.cell.2015.04.025 · Cited by 489
Broad-Spectrum Mildew Resistance in Arabidopsis thaliana Mediated by RPW8
Xiao, S., Ellwood, S., Calis, O., Patrick, E., Li, T., Coleman, M., & Turner, J. G. (2001) · Science · doi:10.1126/science.291.5501.118 · Cited by 475
Evolutionary History and Stress Regulation of Plant Receptor-Like Kinase/Pelle Genes
Lehti-Shiu, M. D., Zou, C., Hanada, K., & Shiu, S.-H. (2009) · Plant Physiology · doi:10.1104/pp.108.134353 · Cited by 446
Integrated genomic and fossil evidence illuminates life’s early evolution and eukaryote origin
Betts, H. C., Puttick, M. N., Clark, J. W., Williams, T. A., Donoghue, P. C. J., & Pisani, D. (2018) · Nature Ecology & Evolution · doi:10.1038/s41559-018-0644-x · Cited by 437
The Evolution of Species Interactions
Thompson, J. N. (1999) · Science · doi:10.1126/science.284.5423.2116 · Cited by 402
Suppression of the MicroRNA Pathway by Bacterial Effector Proteins
Navarro, L., Jay, F., Nomura, K., He, S. Y., & Voinnet, O. (2008) · Science · doi:10.1126/science.1159505 · Cited by 396
Diversity, classification and function of the plant protein kinase superfamily
Lehti-Shiu, M. D., & Shiu, S.-H. (2012) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2012.0003 · Cited by 387
Plant evolution: landmarks on the path to terrestrial life
de Vries, J., & Archibald, J. M. (2018) · New Phytologist · doi:10.1111/nph.14975 · Cited by 379
Burke, C., Thomas, T., Lewis, M., Steinberg, P., & Kjelleberg, S. (2011) · The ISME Journal · doi:10.1038/ismej.2010.164 · Cited by 378
The Evolutionary Origin of a Terrestrial Flora
Delwiche, C. F., & Cooper, E. D. (2015) · Current Biology · doi:10.1016/j.cub.2015.08.029 · Cited by 358
The evolutionary phylogeny of the oomycete “fungi”
Beakes, G. W., Glockling, S. L., & Sekimoto, S. (2011) · PROTOPLASMA · doi:10.1007/s00709-011-0269-2 · Cited by 358
The origin and evolution of mycorrhizal symbioses: from palaeomycology to phylogenomics
Strullu‐Derrien, C., Selosse, M., Kenrick, P., & Martin, F. M. (2018) · New Phytologist · doi:10.1111/nph.15076 · Cited by 352
A Genome-Wide Survey of R Gene Polymorphisms in Arabidopsis
Bakker, E. G., Toomajian, C., Kreitman, M., & Bergelson, J. (2006) · The Plant Cell · doi:10.1105/tpc.106.042614 · Cited by 335
Algal ancestor of land plants was preadapted for symbiosis
Delaux, P.-M., Radhakrishnan, G. V., Jayaraman, D., Cheema, J., Malbreil, M., Volkening, J. D., Sekimoto, H., Nishiyama, T., Melkonian, M., Pokorny, L., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1515426112 · Cited by 334
Running with the Red Queen: the role of biotic conflicts in evolution
Brockhurst, M. A., Chapman, T., King, K. C., Mank, J. E., Paterson, S., & Hurst, G. D. D. (2014) · Proceedings of the Royal Society B: Biological Sciences · doi:10.1098/rspb.2014.1382 · Cited by 332
Is genome size influenced by colonization of new environments in dipteran species?
NARDON, C., DECELIERE, G., LŒVENBRUCK, C., WEISS, M., VIEIRA, C., & BIÉMONT, C. (2005) · Molecular Ecology · doi:10.1111/j.1365-294x.2005.02457.x · Cited by 326
Plant-Parasite Coevolution: Bridging the Gap between Genetics and Ecology
Brown, J. K. M., & Tellier, A. (2011) · Annual Review of Phytopathology · doi:10.1146/annurev-phyto-072910-095301 · Cited by 325
Sarris, P. F., Cevik, V., Dagdas, G., Jones, J. D. G., & Krasileva, K. V. (2016) · BMC Biology · doi:10.1186/s12915-016-0228-7 · Cited by 324
Blanc, G., Agarkova, I., Grimwood, J., Kuo, A., Brueggeman, A., Dunigan, D. D., Gurnon, J., Ladunga, I., Lindquist, E., Lucas, S., et al. (2012) · Genome Biology · doi:10.1186/gb-2012-13-5-r39 · Cited by 317
Leonard, C. J., Aravind, L., & Koonin, E. V. (1998) · Genome Research · doi:10.1101/gr.8.10.1038 · Cited by 317
Shao, Z.-Q., Xue, J.-Y., Wu, P., Zhang, Y.-M., Wu, Y., Hang, Y.-Y., Wang, B., & Chen, J.-Q. (2016) · Plant Physiology · doi:10.1104/pp.15.01487 · Cited by 309
Patterns of Positive Selection in the Complete NBS-LRR Gene Family of Arabidopsis thaliana
Mondragón-Palomino, M., Meyers, B. C., Michelmore, R. W., & Gaut, B. S. (2002) · Genome Research · doi:10.1101/gr.159402 · Cited by 304
Evolutionary insights into host–pathogen interactions from mammalian sequence data
Sironi, M., Cagliani, R., Forni, D., & Clerici, M. (2015) · Nature Reviews Genetics · doi:10.1038/nrg3905 · Cited by 302
Mutualistic mycorrhiza-like symbiosis in the most ancient group of land plants
Humphreys, C. P., Franks, P. J., Rees, M., Bidartondo, M. I., Leake, J. R., & Beerling, D. J. (2010) · Nature Communications · doi:10.1038/ncomms1105 · Cited by 294
Epigenetic variation in Arabidopsis disease resistance
Stokes, T. L., Kunkel, B. N., & Richards, E. J. (2002) · Genes & Development · doi:10.1101/gad.952102 · Cited by 285
Kroj, T., Chanclud, E., Michel-Romiti, C., Grand, X., & Morel, J. (2016) · New Phytologist · doi:10.1111/nph.13869 · Cited by 282
Signature of balancing selection in Arabidopsis
Tian, D., Araki, H., Stahl, E., Bergelson, J., & Kreitman, M. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.172203599 · Cited by 272
Precision of molecular time estimates
Blair Hedges, S., & Kumar, S. (2004) · Trends in Genetics · doi:10.1016/j.tig.2004.03.004 · Cited by 271
Fungal Effector Protein AVR2 Targets Diversifying Defense-Related Cys Proteases of Tomato
Shabab, M., Shindo, T., Gu, C., Kaschani, F., Pansuriya, T., Chintha, R., Harzen, A., Colby, T., Kamoun, S., & van der Hoorn, R. A. L. (2008) · The Plant Cell · doi:10.1105/tpc.107.056325 · Cited by 270
Rose, L. E., Bittner-Eddy, P. D., Langley, C. H., Holub, E. B., Michelmore, R. W., & Beynon, J. L. (2004) · Genetics · doi:10.1534/genetics.166.3.1517 · Cited by 264
The long-term maintenance of a resistance polymorphism through diffuse interactions
Karasov, T. L., Kniskern, J. M., Gao, L., DeYoung, B. J., Ding, J., Dubiella, U., Lastra, R. O., Nallu, S., Roux, F., Innes, R. W., et al. (2014) · Nature · doi:10.1038/nature13439 · Cited by 259
Shine, M. B., Yang, J., El‐Habbak, M., Nagyabhyru, P., Fu, D., Navarre, D., Ghabrial, S., Kachroo, P., & Kachroo, A. (2016) · New Phytologist · doi:10.1111/nph.14078 · Cited by 247
Insights into the Origin and Evolution of the Plant Hormone Signaling Machinery
Wang, C., Liu, Y., Li, S.-S., & Han, G.-Z. (2015) · Plant Physiology · doi:10.1104/pp.114.247403 · Cited by 244
Self-citationRapid genetic change underpins antagonistic coevolution in a natural host‐pathogen metapopulation
Thrall, P. H., Laine, A., Ravensdale, M., Nemri, A., Dodds, P. N., Barrett, L. G., & Burdon, J. J. (2012) · Ecology Letters · doi:10.1111/j.1461-0248.2012.01749.x · Cited by 242
Cai, R., Lewis, J., Yan, S., Liu, H., Clarke, C. R., Campanile, F., Almeida, N. F., Studholme, D. J., Lindeberg, M., Schneider, D., et al. (2011) · PLoS Pathogens · doi:10.1371/journal.ppat.1002130 · Cited by 236
Analysis of Flagellin Perception Mediated by flg22 Receptor OsFLS2 in Rice
Takai, R., Isogai, A., Takayama, S., & Che, F.-S. (2008) · Molecular Plant-Microbe Interactions® · doi:10.1094/mpmi-21-12-1635 · Cited by 226
Robatzek, S., Bittel, P., Chinchilla, D., Köchner, P., Felix, G., Shiu, S.-H., & Boller, T. (2007) · Plant Molecular Biology · doi:10.1007/s11103-007-9173-8 · Cited by 225
Early events in the pathogenicity of Pseudomonas syringae on Nicotiana benthamiana
Hann, D. R., & Rathjen, J. P. (2007) · The Plant Journal · doi:10.1111/j.1365-313x.2006.02981.x · Cited by 218
Early Diverging Fungi: Diversity and Impact at the Dawn of Terrestrial Life
Berbee, M. L., James, T. Y., & Strullu-Derrien, C. (2017) · Annual Review of Microbiology · doi:10.1146/annurev-micro-030117-020324 · Cited by 218
Liu, P.-L., Du, L., Huang, Y., Gao, S.-M., & Yu, M. (2017) · BMC Evolutionary Biology · doi:10.1186/s12862-017-0891-5 · Cited by 209
Do early branching lineages signify ancestral traits?
CRISP, M., & COOK, L. (2005) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2004.11.010 · Cited by 204
Trdá, L., Fernandez, O., Boutrot, F., Héloir, M., Kelloniemi, J., Daire, X., Adrian, M., Clément, C., Zipfel, C., Dorey, S., et al. (2014) · New Phytologist · doi:10.1111/nph.12592 · Cited by 195
Natural Selection for Polymorphism in the Disease Resistance Gene Rps2 of Arabidopsis thaliana
Mauricio, R., Stahl, E. A., Korves, T., Tian, D., Kreitman, M., & Bergelson, J. (2003) · Genetics · doi:10.1093/genetics/163.2.735 · Cited by 192
MicroRNAs Suppress NB Domain Genes in Tomato That Confer Resistance to Fusarium oxysporum
Ouyang, S., Park, G., Atamian, H. S., Han, C. S., Stajich, J. E., Kaloshian, I., & Borkovich, K. A. (2014) · PLoS Pathogens · doi:10.1371/journal.ppat.1004464 · Cited by 188
Zhang, Y., Xia, R., Kuang, H., & Meyers, B. C. (2016) · Molecular Biology and Evolution · doi:10.1093/molbev/msw154 · Cited by 186
Endogenous viruses: Connecting recent and ancient viral evolution
Aiewsakun, P., & Katzourakis, A. (2015) · Virology · doi:10.1016/j.virol.2015.02.011 · Cited by 185
Unusual Life Style of Giant Chlorella Viruses
Van Etten, J. L. (2003) · Annual Review of Genetics · doi:10.1146/annurev.genet.37.110801.143915 · Cited by 183
Chang, Y., Wang, S., Sekimoto, S., Aerts, A. L., Choi, C., Clum, A., LaButti, K. M., Lindquist, E. A., Yee Ngan, C., Ohm, R. A., et al. (2015) · Genome Biology and Evolution · doi:10.1093/gbe/evv090 · Cited by 180
Mukherjee, K., Campos, H., & Kolaczkowski, B. (2013) · Molecular Biology and Evolution · doi:10.1093/molbev/mss263 · Cited by 175
Letcher, P. M., Lopez, S., Schmieder, R., Lee, P. A., Behnke, C., Powell, M. J., & McBride, R. C. (2013) · PLoS ONE · doi:10.1371/journal.pone.0056232 · Cited by 171
Genome-wide patterns of single-feature polymorphism in Arabidopsis thaliana
Borevitz, J., Hazen, S. P., Michael, T. P., Morris, G. P., Baxter, I. R., Hu, T. T., Chen, H., Werner, J. D., Nordborg, M., Salt, D. E., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0705323104 · Cited by 157
Clarke, C. R., Chinchilla, D., Hind, S. R., Taguchi, F., Miki, R., Ichinose, Y., Martin, G. B., Leman, S. C., Felix, G., & Vinatzer, B. A. (2013) · New Phytologist · doi:10.1111/nph.12408 · Cited by 157
RNA-Mediated Silencing in Algae: Biological Roles and Tools for Analysis of Gene Function
Cerutti, H. D., Ma, X., Msanne, J., & Repas, T. (2011) · Eukaryotic Cell · doi:10.1128/ec.05106-11 · Cited by 157
Genomic perspectives on the birth and spread of plastids
Archibald, J. M. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1421374112 · Cited by 156
Revisiting the Origin of Plant NBS-LRR Genes
Shao, Z., Xue, J., Wang, Q., Wang, B., & Chen, J. (2018) · Trends in Plant Science · doi:10.1016/j.tplants.2018.10.015 · Cited by 150
Out of Water: The Origin and Early Diversification of Plant R-Genes
Gao, Y., Wang, W., Zhang, T., Gong, Z. H., Zhao, H., & Han, G. (2018) · PLANT PHYSIOLOGY · doi:10.1104/pp.18.00185 · Cited by 149
Self-citationSensing of molecular patterns through cell surface immune receptors
Ranf, S. (2017) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2017.04.011 · Cited by 145
Martin, W. F. (2017) · BioEssays · doi:10.1002/bies.201700115 · Cited by 144
Fischer, I., Diévart, A., Droc, G., Dufayard, J.-F., & Chantret, N. (2016) · PLANT PHYSIOLOGY · doi:10.1104/pp.15.01470 · Cited by 139
Plants, fungi and oomycetes: a 400‐million year affair that shapes the biosphere
Selosse, M., Strullu‐Derrien, C., Martin, F. M., Kamoun, S., & Kenrick, P. (2015) · New Phytologist · doi:10.1111/nph.13371 · Cited by 136
Xia, R., Xu, J., Arikit, S., & Meyers, B. C. (2015) · Molecular Biology and Evolution · doi:10.1093/molbev/msv164 · Cited by 135
Genomic variability as a driver of plant–pathogen coevolution?
Karasov, T. L., Horton, M., & Bergelson, J. M. (2014) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2013.12.003 · Cited by 133
Rapidly evolving R genes in diverse grass species confer resistance to rice blast disease
Yang, S., Li, J., Zhang, X., Zhang, Q., Huang, J. W., Chen, J., Hartl, D. L., & Tian, D. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1318211110 · Cited by 132
The NBS-LRR architectures of plant R-proteins and metazoan NLRs evolved in independent events
Urbach, J. M., & Ausubel, F. M. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1619730114 · Cited by 131
Contrasted coevolutionary dynamics between a bacterial pathogen and its bacteriophages
Betts, A., Kaltz, O., & Hochberg, M. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1406763111 · Cited by 123
The S phagnum microbiome supports bog ecosystem functioning under extreme conditions
Bragina, A., Oberauner‐Wappis, L., Zachow, C., Halwachs, B., Thallinger, G., Müller, H., & Berg, G. (2014) · Molecular Ecology · doi:10.1111/mec.12885 · Cited by 118
de Vries, J., de Vries, S., Slamovits, C. H., Rose, L. E., & Archibald, J. M. (2017) · Plant and Cell Physiology · doi:10.1093/pcp/pcx037 · Cited by 114
Antagonistic bacteria disrupt calcium homeostasis and immobilize algal cells
Aiyar, P., Schaeme, D., García‐Altares, M., Flores, D. C., Dathe, H., Hertweck, C., Sasso, S., & Mittag, M. (2017) · Nature Communications · doi:10.1038/s41467-017-01547-8 · Cited by 104
Upson, J., Zess, E. K., Białas, A., Wu, C., & Kamoun, S. (2018) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2018.03.003 · Cited by 99
Plant genomes enclose footprints of past infections by giant virus relatives
Maumus, F., Epert, A., Nogué, F., & Blanc, G. (2014) · Nature Communications · doi:10.1038/ncomms5268 · Cited by 97
Frequency-dependent selection in a wild plant-pathogen system
Chaboudez, P., & Burdon, J. J. (1995) · Oecologia · doi:10.1007/bf00341361 · Cited by 87
Flagellin Perception Varies Quantitatively in Arabidopsis thaliana and Its Relatives
Vetter, M., Kronholm, I., He, F., Häweker, H., Reymond, M., Bergelson, J. M., Robatzek, S., & de Meaux, J. (2012) · Molecular Biology and Evolution · doi:10.1093/molbev/mss011 · Cited by 87
de Vries, S., Kloesges, T., & Rose, L. E. (2015) · Genome Biology and Evolution · doi:10.1093/gbe/evv225 · Cited by 85
Evolutionary dynamics of mycorrhizal symbiosis in land plant diversification
Feijen, F. A. A., Vos, R. A., Nuytinck, J., & Merckx, V. S. F. T. (2018) · Scientific Reports · doi:10.1038/s41598-018-28920-x · Cited by 85
Filée, J. (2014) · Virology · doi:10.1016/j.virol.2014.06.004 · Cited by 84
Functional Divergence of Two Secreted Immune Proteases of Tomato
Ilyas, M., Hörger, A. C., Bozkurt, T. O., van den Burg, H. A., Kaschani, F., Kaiser, M., Belhaj, K., Smoker, M., JOOSTEN, M. H. A. J., Kamoun, S., et al. (2015) · Current Biology · doi:10.1016/j.cub.2015.07.030 · Cited by 81
Demystifying Eukaryote Lateral Gene Transfer (Response to Martin 2017 DOI: 10.1002/bies.201700115)
Leger, M. M., Eme, L., Stairs, C. W., & Roger, A. J. (2018) · BioEssays · doi:10.1002/bies.201700242 · Cited by 81
Hörger, A. C., Ilyas, M., Stephan, W., Tellier, A., van der Hoorn, R. A. L., & Rose, L. E. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1002813 · Cited by 79
Burdon, J. J., & Thrall, P. H. (2013) · European Journal of Plant Pathology · doi:10.1007/s10658-013-0265-9 · Cited by 77
Genomics-Informed Insights into Endosymbiotic Organelle Evolution in Photosynthetic Eukaryotes
Nowack, E. C. M., & Weber, A. P. M. (2018) · Annual Review of Plant Biology · doi:10.1146/annurev-arplant-042817-040209 · Cited by 74
The monoplastidic bottleneck in algae and plant evolution
de Vries, J., & Gould, S. B. (2017) · Journal of Cell Science · doi:10.1242/jcs.203414 · Cited by 70
On plant defense signaling networks and early land plant evolution
de Vries, S., de Vries, J., von Dahlen, J. K., Gould, S. B., Archibald, J. M., Rose, L. E., & Slamovits, C. H. (2018) · Communicative & Integrative Biology · doi:10.1080/19420889.2018.1486168 · Cited by 65
Oomycetes and fungi: important parasites on marine algae
Li, W., Zhang, T.-Y., Tang, X., & Wang, B. (2010) · Acta Oceanologica Sinica · doi:10.1007/s13131-010-0065-4 · Cited by 60
Albert, M., Jehle, A. K., Lipschis, M., Mueller, K., Zeng, Y., & Felix, G. (2010) · European Journal of Cell Biology · doi:10.1016/j.ejcb.2009.11.015 · Cited by 59
Sasaki, G., Katoh, K., Hirose, N., Suga, H., Kuma, K., Miyata, T., & Su, Z.-H. (2007) · Gene · doi:10.1016/j.gene.2007.07.009 · Cited by 56
Genetic architecture and pleiotropy shape costs of Rps2-mediated resistance in Arabidopsis thaliana
MacQueen, A., Sun, X., & Bergelson, J. M. (2016) · Nature Plants · doi:10.1038/nplants.2016.110 · Cited by 53
Wheeler, G. L., Miranda‐Saavedra, D., & Barton, G. J. (2008) · Genetics · doi:10.1534/genetics.107.085936 · Cited by 45
de Vries, S., Kukuk, A., von Dahlen, J. K., Schnake, A., Kloesges, T., & Rose, L. E. (2018) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2017.2560 · Cited by 45
Arnaud‐Haond, S., Aires, T., Candeias, R., Teixeira, S., Duarte, C. M., Valéro, M., & Serrão, E. Á. (2017) · Molecular Ecology · doi:10.1111/mec.14030 · Cited by 40
A Genomic Perspective on the Generation and Maintenance of Genetic Diversity in Herbivorous Insects
Gloss, A. D., Groen, S. C., & Whiteman, N. K. (2016) · Annual Review of Ecology Evolution and Systematics · doi:10.1146/annurev-ecolsys-121415-032220 · Cited by 39
Changes in the composition of the RNA virome mark evolutionary transitions in green plants
Mushegian, A. R., SHIPUNOV, A. B., & Elena, S. F. (2016) · BMC Biology · doi:10.1186/s12915-016-0288-8 · Cited by 39
de Vries, S., von Dahlen, J. K., Uhlmann, C., Schnake, A., Kloesges, T., & Rose, L. E. (2016) · Molecular Plant Pathology · doi:10.1111/mpp.12465 · Cited by 27
Euphyllophyte Paleoviruses Illuminate Hidden Diversity and Macroevolutionary Mode of Caulimoviridae
Gong, Z. H., & Han, G. (2018) · Journal of Virology · doi:10.1128/jvi.02043-17 · Cited by 27
Self-citation(1982)
Cited by
Plant-associated fungi co-opt ancient antimicrobials for host manipulation
Mesny, F., Wolf, V., López-Moral, A., Kraege, A., Punt, W., Liu, S., Zhu, J., Park, J., Sato, Y., & Thomma, B. P. H. J. (2026) · Science Advances · doi:10.1126/sciadv.aec1406 · Cited by 11
Metadata
- Authors
- Han, G.
- Venue
- New Phytologist
- Publisher
- Wiley
- Published
- 2019-01-07
- Volume
- 222
- Issue
- 1
- Pages
- 70-83
- ISSN
- 0028-646X (ISSN-L)
- 1469-8137
- OpenAlex
- W2906224520
- Cited by
- 282
- References
- 159
- FWCI
- 20.23
- Type
- journal article
- Language
- en
- Open access
- bronze
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
Data sources
Bibliographic data: Semantic Scholar, OpenAlex, Crossref.
Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).
Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.
