Analysis of a Plant Complex Resistance Gene Locus Underlying Immune-Related Hybrid Incompatibility and Its Occurrence in Nature

English version České info

In plants, naturally evolving disease resistance (R) genes can cause autoimmunity when combined with different genetic backgrounds. This phenomenon, called immune-related hybrid incompatibility (HI), leads to growth inhibition and fitness loss due to inappropriate activation of defense. HI likely reflects different evolutionary paths of immune-related genes in nature. We have examined the genetic architecture of a complex R locus present in a Central European accession (Ler) which underlies HI with Central Asian accessions of Arabidopsis. We show that expression of one gene (R3) within the Ler cluster of eight tandem R genes (R1–R8) controls the balance between growth and defense but that R3 needs at least one other co-acting member within the R locus to condition HI. We traced the R1–R8 haplotype to a local population of Ler relatives in Poland where it also underlies HI with Central Asian accessions. Occurrence of the incompatible haplotype in ∼30% of genetically diverse local individuals, suggests that it has not arisen recently and has been maintained through selection or drift. Co-occurrence in the same population of individuals containing different R genes that do not cause HI provides a basis for determining genetic and environmental forces influencing how plant immunity genes evolve and diversify.

Vyšlo v časopise: Analysis of a Plant Complex Resistance Gene Locus Underlying Immune-Related Hybrid Incompatibility and Its Occurrence in Nature. PLoS Genet 10(12): e32767. doi:10.1371/journal.pgen.1004848
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004848

Souhrn

Zdroje

1. LososJB, ArnoldSJ, BejeranoG, BrodieED, HibbettD, et al. (2013) Evolutionary biology for the 21st century. PLoS Biol 11: e1001466 doi:10.1371/journal.pbio.1001466

2. RiesebergLH, WillisJH (2007) Plant speciation. Science 317: 910–914 doi:10.1126/science.1137729

3. BombliesK (2010) Doomed lovers: mechanisms of isolation and incompatibility in plants. Annu Rev Plant Biol 61: 109–124 doi:10.1146/annurev-arplant-042809-112146

4. AbbottR, AlbachD, AnsellS, ArntzenJW, BairdSJE, et al. (2013) Hybridization and speciation. J Evol Biol 26: 229–246 doi:10.1111/j.1420-9101.2012.02599.x

5. OuyangY, LiuY-G, ZhangQ (2010) Hybrid sterility in plant: stories from rice. Curr Opin Plant Biol 13: 186–192 doi:10.1016/j.pbi.2010.01.002

6. BombliesK, LempeJ, EppleP, WarthmannN, LanzC, et al. (2007) Autoimmune response as a mechanism for a Dobzhansky-Muller-type incompatibility syndrome in plants. PLoS Biol 5: e236 doi:10.1371/journal.pbio.0050236

7. MacNairMR, ChristieP (1983) Reproductive isolation as a pleiotropic effect of copper tolerance in Mimulus guttatus? Heredity (Edinb) 50: 295–302 doi:10.1038/hdy.1983.31

8. BikardD, PatelD, Le MettéC, GiorgiV, CamilleriC, et al. (2009) Divergent evolution of duplicate genes leads to genetic incompatibilities within A. thaliana. Science 323: 623–626 doi:10.1126/science.1165917

9. ClarkRM, SchweikertG, ToomajianC, OssowskiS, ZellerG, et al. (2007) Common sequence polymorphisms shaping genetic diversity in Arabidopsis thaliana. Science 317: 338–342 doi:10.1126/science.1138632

10. BombliesK, WeigelD (2007) Hybrid necrosis: autoimmunity as a potential gene-flow barrier in plant species. Nat Rev Genet 8: 382–393 doi:10.1038/nrg2082

11. DoddsPN, RathjenJP (2010) Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet 11: 539–548 doi:10.1038/nrg2812

12. GuoY-L, FitzJ, SchneebergerK, OssowskiS, CaoJ, et al. (2011) Genome-wide comparison of nucleotide-binding site-leucine-rich repeat-encoding genes in Arabidopsis. Plant Physiol 157: 757–769 doi:10.1104/pp.111.181990

13. JonesJDG, DanglJL (2006) The plant immune system. Nature 444: 323–329 doi:10.1038/nature05286

14. KarasovTL, HortonMW, BergelsonJ (2014) Genomic variability as a driver of plant-pathogen coevolution? Curr Opin Plant Biol 18: 24–30 doi:10.1016/j.pbi.2013.12.003

15. SalvaudonL, GiraudT, ShykoffJA (2008) Genetic diversity in natural populations: a fundamental component of plant-microbe interactions. Curr Opin Plant Biol 11: 135–143 doi:10.1016/j.pbi.2008.02.002

16. StahlEA, DwyerG, MauricioR, KreitmanM, BergelsonJ (1999) Dynamics of disease resistance polymorphism at the RPM1 locus of Arabidopsis. Nature 400: 667–671 doi:10.1038/23260

17. MukhtarMS, CarvunisA-R, DrezeM, EppleP, SteinbrennerJ, et al. (2011) Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science 333: 596–601 doi:10.1126/science.1203659

18. AlcázarR, ParkerJE (2011) The impact of temperature on balancing immune responsiveness and growth in Arabidopsis. Trends Plant Sci 16: 666–675 doi:10.1016/j.tplants.2011.09.001

19. MeyersBC, KaushikS, NandetyRS (2005) Evolving disease resistance genes. Curr Opin Plant Biol 8: 129–134 doi:10.1016/j.pbi.2005.01.002

20. WickerT, YahiaouiN, KellerB (2007) Illegitimate recombination is a major evolutionary mechanism for initiating size variation in plant resistance genes. Plant J 51: 631–641 doi:10.1111/j.1365-313X.2007.03164.x

21. JacobF, VernaldiS, MaekawaT (2013) Evolution and conservation of plant NLR functions. Front Immunol 4: 297 doi:10.3389/fimmu.2013.00297

22. CaoJ, SchneebergerK, OssowskiS, GüntherT, BenderS, et al. (2011) Whole-genome sequencing of multiple Arabidopsis thaliana populations. Nat Genet 43: 956–963 doi:10.1038/ng.911

23. AlcázarR, GarcíaAV, KronholmI, de MeauxJ, KoornneefM, et al. (2010) Natural variation at Strubbelig Receptor Kinase 3 drives immune-triggered incompatibilities between Arabidopsis thaliana accessions. Nat Genet 42: 1135–1139 doi:10.1038/ng.704

24. TahirJ, WatanabeM, JingH-C, HunterDA, TohgeT, et al. (2012) Activation of R-mediated innate immunity and disease susceptibility is affected by mutations in a cytosolic O-acetylserine (thiol) lyase in Arabidopsis. Plant J doi:10.1111/tpj.12021

25. JeukenMJW, ZhangNW, McHaleLK, PelgromK, den BoerE, et al. (2009) RIN4 causes hybrid necrosis and race-specific resistance in an interspecific lettuce hybrid. Plant Cell 21: 3368–3378 doi:10.1105/tpc.109.070334

26. YamamotoE, TakashiT, MorinakaY, LinS, WuJ, et al. (2010) Gain of deleterious function causes an autoimmune response and Bateson-Dobzhansky-Muller incompatibility in rice. Mol Genet Genomics 283: 305–315 doi:10.1007/s00438-010-0514-y

27. ChenC, ChenH, LinY-S, ShenJ-B, ShanJ-X, et al. (2014) A two-locus interaction causes interspecific hybrid weakness in rice. Nat Commun 5: 3357 doi:10.1038/ncomms4357

28. SangsterTA, SalathiaN, LeeHN, WatanabeE, SchellenbergK, et al. (2008) HSP90-buffered genetic variation is common in Arabidopsis thaliana. Proc Natl Acad Sci U S A 105: 2969–2974 doi:10.1073/pnas.0712210105

29. BotellaMA, ParkerJE, FrostLN, Bittner-EddyPD, BeynonJL, et al. (1998) Three genes of the Arabidopsis RPP1 complex resistance locus recognize distinct Peronospora parasitica avirulence determinants. Plant Cell 10: 1847–1860.

30. RehmanyAP, GordonA, RoseLE, AllenRL, ArmstrongMR, et al. (2005) Differential recognition of highly divergent downy mildew avirulence gene alleles by RPP1 resistance genes from two Arabidopsis lines. Plant Cell 17: 1839–1850 doi:10.1105/tpc.105.031807

31. AlcázarR, GarcíaAV, ParkerJE, ReymondM (2009) Incremental steps toward incompatibility revealed by Arabidopsis epistatic interactions modulating salicylic acid pathway activation. Proc Natl Acad Sci U S A 106: 334–339 doi:10.1073/pnas.0811734106

32. HuTT, PattynP, BakkerEG, CaoJ, ChengJ-F, et al. (2011) The Arabidopsis lyrata genome sequence and the basis of rapid genome size change. Nat Genet 43: 476–481 doi:10.1038/ng.807

33. TianD, TrawMB, ChenJQ, KreitmanM, BergelsonJ (2003) Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 423: 74–77 doi:10.1038/nature01588

34. Van HultenM, PelserM, van LoonLC, PieterseCMJ, TonJ (2006) Costs and benefits of priming for defense in Arabidopsis. Proc Natl Acad Sci U S A 103: 5602–5607 doi:10.1073/pnas.0510213103

35. SinapidouE, WilliamsK, NottL, BahktS, TörM, et al. (2004) Two TIR:NB:LRR genes are required to specify resistance to Peronospora parasitica isolate Cala2 in Arabidopsis. Plant J 38: 898–909 doi:10.1111/j.1365-313X.2004.02099.x

36. el-LithyME, BentsinkL, HanhartCJ, RuysGJ, RovitoD, et al. (2006) New Arabidopsis recombinant inbred line populations genotyped using SNPWave and their use for mapping flowering-time quantitative trait loci. Genetics 172: 1867–1876 doi:10.1534/genetics.105.050617

37. KranzA, KirchheimB (1987) Genetic resources in Arabidopsis. Arab Inf Serv 24: 160–161.

38. WarthmannN, FitzJ, WeigelD (2007) MSQT for choosing SNP assays from multiple DNA alignments. Bioinformatics 23: 2784–2787 doi:10.1093/bioinformatics/btm428

39. PlattA, HortonM, HuangYS, LiY, AnastasioAE, et al. (2010) The scale of population structure in Arabidopsis thaliana. PLoS Genet 6: e1000843 doi:10.1371/journal.pgen.1000843

40. BombliesK, YantL, LaitinenRA, KimS-T, HollisterJD, et al. (2010) Local-scale patterns of genetic variability, outcrossing, and spatial structure in natural stands of Arabidopsis thaliana. PLoS Genet 6: e1000890 doi:10.1371/journal.pgen.1000890

41. FalushD, StephensM, PritchardJK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164: 1567–1587.

42. LeisterD (2004) Tandem and segmental gene duplication and recombination in the evolution of plant disease resistance gene. Trends Genet 20: 116–122.

43. McDowellJM, SimonSA (2006) Recent insights into R gene evolution. Mol Plant Pathol 7: 437–448 doi:10.1111/j.1364-3703.2006.00342.x

44. CoatesME, BeynonJL (2010) Hyaloperonospora arabidopsidis as a pathogen model. Annu Rev Phytopathol 48: 329–345 doi:10.1146/annurev-phyto-080508-094422

45. ChinDB, Arroyo-GarciaR, OchoaOE, KesseliRV, LavelleDO, et al. (2001) Recombination and spontaneous mutation at the major cluster of resistance genes in lettuce (Lactuca sativa). Genetics 157: 831–849.

46. TodescoM, BalasubramanianS, HuTT, TrawMB, HortonM, et al. (2010) Natural allelic variation underlying a major fitness trade-off in Arabidopsis thaliana. Nature 465: 632–636 doi:10.1038/nature09083

47. SchmitzRJ, SchultzMD, UrichMA, NeryJR, PelizzolaM, et al. (2013) Patterns of population epigenomic diversity. Nature 495: 193–198 doi:10.1038/nature11968

48. YuA, LepèreG, JayF, WangJ, BapaumeL, et al. (2013) Dynamics and biological relevance of DNA demethylation in Arabidopsis antibacterial defense. Proc Natl Acad Sci U S A 110: 2389–2394 doi:10.1073/pnas.1211757110

49. BoccaraM, SarazinA, ThiébeauldO, JayF, VoinnetO, et al. (2014) The Arabidopsis miR472-RDR6 silencing pathway modulates PAMP- and effector-triggered immunity through the post-transcriptional control of disease resistance genes. PLoS Pathog 10: e1003883 doi:10.1371/journal.ppat.1003883

50. GloggnitzerJ, AkimchevaS, SrinivasanA, KusendaB, RiehsN, et al. (2014) Nonsense-mediated mRNA decay modulates immune receptor levels to regulate plant antibacterial defense. Cell Host Microbe 16: 376–390 doi:10.1016/j.chom.2014.08.010

51. TackAJM, ThrallPH, BarrettLG, BurdonJJ, LaineA-L (2012) Variation in infectivity and aggressiveness in space and time in wild host-pathogen systems: causes and consequences. J Evol Biol 25: 1918–1936 doi:10.1111/j.1420-9101.2012.02588.x

52. ThrallPH, LaineA-L, RavensdaleM, NemriA, DoddsPN, et al. (2012) Rapid genetic change underpins antagonistic coevolution in a natural host-pathogen metapopulation. Ecol Lett 15: 425–435 doi:10.1111/j.1461-0248.2012.01749.x

53. GandonS (2002) Local adaptation and the geometry of host-parasite coevolution. Ecol Lett 5: 246–256 doi:10.1046/j.1461-0248.2002.00305.x

54. McDowellJM, DhandaydhamM, LongTA, AartsMG, GoffS, et al. (1998) Intragenic recombination and diversifying selection contribute to the evolution of downy mildew resistance at the RPP8 locus of Arabidopsis. Plant Cell 10: 1861–1874.

55. BulgarelliD, RottM, SchlaeppiK, Ver Loren van ThemaatE, AhmadinejadN, et al. (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488: 91–95 doi:10.1038/nature11336

56. OssowskiS, SchwabR, WeigelD (2008) Gene silencing in plants using artificial microRNAs and other small RNAs. Plant J 53: 674–690 doi:10.1111/j.1365-313X.2007.03328.x

57. CloughSJ, BentAF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735–743 doi:10.1046/j.1365-313x.1998.00343.x

58. KonczC, SchellJ (1986) The promoter of TL-DNA gene 5 controls the tissue-specific expression of chimaeric genes carried by a novel type of Agrobacterium binary vector. MGG Mol Gen Genet 204: 383–396 doi:10.1007/BF00331014

59. EvannoG, RegnautS, GoudetJ (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14: 2611–2620 doi:10.1111/j.1365-294X.2005.02553.x

60. HusonDH, BryantD (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23: 254–267 doi:10.1093/molbev/msj030

61. LibradoP, RozasJ (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451–1452 doi:10.1093/bioinformatics/btp187