Expression profiling across wild and cultivated tomatoes supports the relevance of early miR482/2118 suppression for Phytophthora resistance

Proceedings of the Royal Society B: Biological Sciences

Volumn 285, Issue 1873, 2018, Pages

  De Vries, Sophie ^a,b   Kukuk, Andreas ^b   von Dahlen, Janina K ^b   Schnake, Anika ^b   Kloesges, Thorsten ^b   Rose, Laura E ^b,c  

^a DALHOUSIE UNIVERSITY   (Canada)

^b HEINRICH HEINE UNIVERSITY   (Germany)

^c Heinrich Heine Universität and Cluster of Excellence on Plant Sciences   (Germany)

Author keywords

Evolution; miRNA signalling; Plant immunity; Solanum

Indexed keywords

COEVOLUTION; CULTIVATION; DISEASE RESISTANCE; FUNGUS; GENE EXPRESSION; GENETIC ENGINEERING; HERB; IMMUNITY; PROTEIN; WILD POPULATION;

LYCOPERSICON; LYCOPERSICON ESCULENTUM; PHYTOPHTHORA; PHYTOPHTHORA INFESTANS; SOLANUM;

MICRORNA; PLANT RNA;

COEVOLUTION; DISEASE RESISTANCE; GENETICS; MICROBIOLOGY; PHYSIOLOGY; PHYTOPHTHORA; PLANT DISEASE; TOMATO;

BIOLOGICAL COEVOLUTION; DISEASE RESISTANCE; LYCOPERSICON ESCULENTUM; MICRORNAS; PHYTOPHTHORA; PLANT DISEASES; RNA, PLANT;

EID: 85043573348     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2017.2560     Document Type: Article

References (53)

1. Whisson SC et al. 2007 A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature 450, 115-118. (doi: 10.1038/ nature06203)
2. Fabro G et al. 2011 Multiple candidate effectors from the oomycete pathogen Hyaloperonospora arabidopsidis suppress host plant immunity. PLoS Pathog. 7, e1002348. (doi10.1371/journal.ppat.1002348)
3. Allen RL, Bittner-Eddy PD, Grenville-Briggs LJ, Meitz JC, Rose LE, Beynon JL. 2004 Host-parasite coevolutionary conflict between Arabidopsis and downy mildew. Science 306, 1957-1960. (doi: 10.1126/science.1104022)
4. Krasileva KV, Dahlbeck D, Staskawicz BJ. 2010 Activation of an Arabidopsis resistance protein is specified by the in planta association of its leucinerich repeat domain with the cognate oomycete effector. Plant Cell 22, 2444-2458. (doi: 10.1105/ tpc.110.075358)
5. Stokes TL, Kunkel BN, Richards EJ. 2002 Epigenetic variation in Arabidopsis disease resistance. Gene. Dev. 16, 171-182. (doi: 10.1101/ gad.952102)
6. Li Y, Yang S, Yang H, Hua J. 2007 The TIR-NB-LRR gene SNC1 is regulated at the transcript level by multiple factors. Mol. Plant Microbe Interact. 20, 1449-1456. (doi: 10.1094/MPMI-20-11-1449)
7. Holt BF, Belkhadier Y, Dangl JL. 2005 Antagonistic control of disease resistance protein stability in the plant immune system. Science 309, 929-932. (doi: 10.1126/science.1109977)
8. Li X, Kapos P, Zhang Y. 2015 NLRs in plants. Curr. Opin. Immunol. 32, 114-121. (doi: 10.1016/j.coi. 2015.01.014)
9. Lai Y, Eulgem T. In press. Transcript-level expression control of plant NLR genes. Mol. Plant Pathol. (doi: 10.1111/mpp.12607)
10. Fei Q, Xia R, Meyers BC. 2013 Phased, secondary, small interfering RNAs in posttranscriptional regulatory networks. Plant Cell 25, 2400-2415. (doi: 10.1105/tpc.113.114652)
11. Zhai J et al. 2011 MicroRNAs as master regulators of the plant NB-LRR defense gene family via the production of phased, trans-acting siRNAs. Gene. Dev. 25, 2540-2553. (doi: 10.1101/gad.177527.111)
12. Li F, Pignatta D, Brunkard JO, Cohn MM, Tung J, Sun H, Kumar P, Baker B. 2012 MicroRNA regulation of plant innate immune receptors. Proc. Natl Acad. Sci. USA 109, 1790-1795. (doi: 10.1073/pnas.1118282109)
13. Shivaprasad PV, Chen HM, Patel K, Bond DM, Santos BA, Baulcombe DC. 2012 A microRNA superfamily regulates nucleotide binding site-leucine-rich repeats and other mRNAs. Plant Cell 24, 859-874. (doi: 10.1105/tpc.111.095380)
14. Ouyang S, Park G, Atamian HS, Han CS, Stajich JE, Kaloshian I, Borkovich KA. 2014 MicroRNAs suppress NB domain genes in tomato that confer resistance to Fusarium oxysporum. PLoS Pathog. 10, e1004464. (doi10.1371/journal.ppat.1004464)
15. de Vries S, Kloesges T, Rose LE. 2015 Evolutionarily dynamic, but robust, targeting of resistance genes by the miR482/2118 gene family in the Solanaceae. Genome Biol. Evol. 7, 3307-3321. (doi: 10.1093/ gbe/evv225)
16. Zhang Y, Xia R, Kuang H, Meyers BC. 2016 The diversification of plant NBS-LRR defense genes directs the evolution of microRNAs that target them. Mol. Biol. Evol. 33, 2692-2705. (doi: 10.1093/ molbev/msw154)
17. Garry G, Forbes GA, Salas A, Santa Cruz M, Perez WG, Nelson RJ. 2005 Genetic diversity and host differentiation among isolates of Phytophthora infestans from cultivated potato and wild solanaceous hosts in Peru. Plant Pathol. 54, 740-748. (doi: 10.1111/j.1365-3059.2005.01250.x)
18. Smart CD, Tanksley SD, Mayton H, Fry W. 2007 Resistance to Phytophthora infestans in Lycopersicon pennellii. Plant Dis. 91, 1045-1049. (doi: 10.1094/ PDIS-91-8-1045)
19. Li J et al. 2011 Identification and mapping of quantitative resistance to late blight (Phytophthora infestans) in Solanum habrochaites LA1777. Euphytica 179, 427-438. (doi: 10.1007/s10681-010-0340-7)
20. Vleeshouwers VGAA, van Dooijeweert W, Govers F, Kamoun S, Colon LT. 2000 The hypersensitive response is associated with host and nonhost resistance to Phytophthora infestans. Planta 210, 853-864. (doi: 10.1007/s004250050690)
21. Fooland MR, Sullenberger MT, Ashrafi H. 2015 Detached-leaflet evaluation of tomato germplasm for late blight resistance and its correspondence to field and greenhouse screenings. Plant Dis. 99, 718-722. (doi: 10.1094/PDIS-08-14-0794-RE)
22. Michalska AM, Sobkowiak S, Flis B, Zimnoch-Guzowska E. 2016 Virulence and aggressiveness of Phytophthora infestans isolates collected in Poland from potato and tomato plants identified no strong specificity. Eur. J. Plant Pathol. 144, 325-336. (doi: 10.1007/s10658-015-0769-6)
23. Zhang C et al. 2014 The Ph-3 gene from Solanum pimpinellifolium encodes CC-NBS-LRR protein conferring resistance to Phytophthora infestans. Theor. Appl. Genet. 127, 1353-1364. (doi: 10.1007/ s00122-014-2303-1)
24. Haas BJ et al. 2009 Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461, 393-398. (doi: 10.1038/ nature08358)
25. Xiong Q, Ye W, Choi D, Wong J, Qiao Y, Tao K, Wang Y, Ma W. 2014 Phytophthora suppressor of RNA silencing 2 is a conserved RxLR effector that promotes infection in soybean and Arabidopsis thaliana. Mol. Plant Microbe Interact. 27, 1379-1389. (doi: 10.1094/MPMI-06-14-0190-R)
26. Vetukuri RR, Whisson SC, Grenville-Briggs LJ. 2017 Phytophthora infestans effector Pi4054 is a novel candidate suppressor of host silencing mechanisms. Eur. J. Plant Pathol. 149, 771-777. (doi: 10.1007/ s10658-017-1222-9)
27. Murashige T, Skoog F. 1962 A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol. Plant. 15, 473-497. (doi: 10.1111/ j.1399-3054.1962.tb08052.x)
28. Caten CE, Jinks JL. 1968 Spontaneous variability of single isolates of Phytophthora infestans. I. Cultural variation. Can J. Bot. 46, 329-348. (doi: 10.1139/ b68-055)
29. de Vries S, von Dahlen JK, Uhlmann C, Schnake A, Kloesges T, Rose LE. 2017 Signatures of selection and host-adapted gene expression of the Phytophthora infestans RNA silencing suppressor PSR2. Mol. Plant Pathol. 18, 110-124. (doi: 10. 1111/mpp.12465)
30. Kruskal WH, Wallis WA. 1952 Use of ranks in onecriterion variance analysis. J. Am. Stat. Assoc. 47, 583-621. (doi: 10.2307/2280779)
31. Sachs L. 1997 Angewandte statistik, pp. 395-397, 662-664. Berlin, Germany: Springer.
32. Shapiro SS, Wilk MB. 1965 An analysis of variance test for normality (complete samples). Biometrika 52, 591-611. (doi: 10.2307/2333709)
33. Mann HB, Whitney DR. 1947 On a test of whether one of two random variables is stochastically larger than the other. Ann. Math. Stat. 18, 50-60. (doi: 10.1214/aoms/1177730491)
34. Gruber AR, Lorenz R, Bernhart SH, Neuböck R, Hofacker IL. 2008 The Vienna RNA Websuite. Nucleic Acids Res. 36, W70-W74. (doi10.1093/nar/ gkn188)
35. Pfaffl MW, Tichopad A, Prgomet C, Neuvians TP. 2004 Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper-Excel-based tool using pair-wise correlations. Biotechnol. Lett. 26, 509-515. (doi: 10.1023/B: BILE.0000019559.84305.47)
36. Pfaffl MW. 2001 A new mathematical model for relative quantification in real-time RTPCR. Nucleic Acids Res. 29, e45. (doi10.1093/nar/ 29.9.e45)
37. Song J et al. 2003 Gene RB cloned from Solanum bulbocastanum confers broad spectrum resistance to potato late blight. Proc. Natl Acad. Sci. USA 100, 9128-9133. (doi: 10.1073/pnas.1533501100)
38. Zhang C et al. 2013 Fine mapping of the Ph-3 gene conferring resistance to late blight (Phytophthora infestans) in tomato. Theor. Appl. Genet. 126, 2643-2653. (doi: 10.1007/s00122-013-2162-1)
39. Lopez-Gomollon S, Mohorianu I, Szittya G, Moulton V, Dalmay T. 2012 Diverse correlation patterns between microRNAs and their targets during tomato fruit development indicates different modes of microRNA actions. Planta 236, 1875-1887. (doi: 10.1007/s00425-012-1734-7)
40. Laxman N, Rubin C-J, Mallmin H, Nilsson O, Pastinen T, Grundberg E, Kindmark A. 2015 Global miRNA expression and correlation with mRNA levels in primary human bone cells. RNA 21, 1433-1443. (doi: 10.1261/rna.049148.114)
41. Wen M, Xie M, Wang Y, Shi S, Tang T. 2016 Expression variations of miRNAs and mRNAs in rice (Oryza sativa). Genome Biol. Evol. 8, 3529-3544. (doi: 10.1093/gbe/evw252)
42. Aukerman MJ, Sakai H. 2003 Regulation of flowering time and floral organ indentity by a microRNA and its APETALA2-like target genes. Plant Cell 15, 2730-2741. (doi: 10.1105/tpc.016238)
43. McDonald BA, Stukenbrock EH. 2016 Rapid emergence of pathogens in agro-ecosystems: global threats to agricultural sustainability and food security. Phil. Trans. R. Soc. B 371, 20160026. (doi: 10.1098/rstb.2016.0026)
44. Moyle LC. 2008 Ecological and evolutionary genomics in the wild tomatoes (Solanum sect. Lycopersicon). Evolution 62, 2995-3013. (doi: 10. 1111/j.1558-5646.2008.00487.x)
45. Tooley PW, Therrien CD, Ritch DL. 1989 Mating type, race composition, nuclear DNA content, and isozyme analysis of Peruvian isolates of Phytophthora infestans. Phytopathology 79, 478-481. (doi: 10.1094/Phyto-79-478)
46. Forbes GA, Escobar XC, Ayala CC, Revelo J, Ordoñez ME, Fry BA, Doucett K, Fry WE. 1997 Population genetic structure of Phytophthora infestans in Ecuador. Phytopathology 87, 375-380. (doi: 10. 1094/PHYTO.1997.87.4.375)
47. Acuña I, Sagredo B, Gutiérez M, Sandoval C, Fahrenkrog A, Secor G, Rivera V, Mancilla S. 2012 Characterization of Phytophthora infestans population in Chile. In Proceedings of the thirteenth EuroBlight workshop, St Petersburg, Russia (ed. HTAM Schepers), pp. 145-150. Wageningen, the Netherlands: DLO Foundation.
48. Moreau P, Thoquet P, Olivier J, Laterrot H, Grimsley N. 1998 Genetic mapping of Ph-2, a single locus controlling partial resistance to Phytophthora infestans in tomato. Mol. Plant Microbe Interact. 11, 259-269. (doi: 10.1094/MPMI.1998.11.4.259)
49. Schoina C, Bouwmeester K, Govers F. 2017 Infection of a tomato cell culture by Phytophthora infestans; a versatile tool to study Phytophthora-host interactions. Plant Methods 13, 88. (doi: 10.1186/ s13007-017-0240-0)
50. Qiao Y et al. 2013 Oomycete pathogens encode RNA silencing suppressors. Nat. Genet. 45, 330-333. (doi: 10.1038/ng.2525)
51. Luan Y, Cui J, Li J, Jiang N, Liu P, Meng J. 2017 Effective enhancement of resistance to Phytophthora infestans by overexpression of miR172a and b in Solanum lycopersicum. Planta 247, 127-138. Early Access Online Version. (doi: 10.1007/s00425-017-2773-x)
52. Kanneganti TD, Huitema E, Cakir C, Kamoun S. 2006 Synergistic interactions of the plant cell death pathways induced by Phytophthora infestans NepIlike protein PiNPP1.1 and INF1 elicitin. Mol. Plant Microbe Interact. 19, 854-863. (doi: 10.1094/MPMI-19-0854)
53. Kelley BS, Lee SJ, Damasceno CM, Chakravarthy S, Kim BD, Martin GB, Rose JK. 2010 A secreted effector protein (SNE1) from Phytophthora infestans is broadly acting suppressor of programmed cell death. Plant J. 62, 357-366. (doi: 10.1111/j.1365-313X.2010.04160.x)