Phytophthora palmivora establishes tissue-specific intracellular infection structures in the earliest divergent land plant lineage

Proceedings of the National Academy of Sciences of the United States of America

Volumn 115, Issue 16, 2018, Pages E3846-E3855

  Carella, Philip ^a   Gogleva, Anna ^a   Tomaselli, Marta ^a   Alfs, Carolin ^a   Schornack, Sebastian ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Bryophyte; Haustoria; Liverworts; Oomycetes; Phytophthora

Indexed keywords

SYNTAXIN;

ARTICLE; CELL INTERACTION; CELL MIGRATION; CONTROLLED STUDY; FEMALE; FUNGAL COLONIZATION; FUNGAL VIRULENCE; HAUSTORIUM; LIVERWORT; MALE; MARCHANTIA; MARCHANTIA POLYMORPHA; MOSS; NONHUMAN; PHOTOSYNTHESIS; PHYTOPHTHORA; PHYTOPHTHORA PALMIVORA; PLANT DISEASE; PLANT FUNGUS INTERACTION; PLANT PATHOGEN INTERACTION; PLANT TISSUE; PRIORITY JOURNAL; PROTEIN TRANSPORT; FUNGUS HYPHAE; MICROBIOLOGY; PATHOGENICITY; SYMBIOSIS; ULTRASTRUCTURE;

HYPHAE; MARCHANTIA; PHYTOPHTHORA; PLANT DISEASES; SYMBIOSIS;

EID: 85045508293     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1717900115     Document Type: Article

References (78)

1. Remy W, Taylor TN, Hass H, Kerp H (1994) Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proc Natl Acad Sci USA 91:11841–11843.
2. Taylor TN, Remy W, Hass H, Kerp H (1995) Fossil arbuscular mycorrhizae from the Early Devonian. Mycologia 87:560–573.
3. Krings M, et al. (2007) Fungal endophytes in a 400-million-yr-old land plant: infection pathways, spatial distribution, and host responses. New Phytol 174:648–657.
4. Strullu-Derrien C, et al. (2014) Fungal associations in Horneophyton ligneri from the Rhynie Chert (c. 407 million year old) closely resemble those in extant lower land plants: novel insights into ancestral plant-fungus symbioses. New Phytol 203:964–979.
5. Ligrone R, et al. (2007) Glomeromycotean associations in liverworts: a molecular, cellular, and taxonomic analysis. Am J Bot 94:1756–1777.
6. Adams DG, Duggan PS (2008) Cyanobacteria-bryophyte symbioses. J Exp Bot 59:1047–1058.
7. Pressel S, Bidartondo MI, Ligrone R, Duckett JG (2010) Fungal symbioses in bryophytes: New insights in the twenty first century. Phytotaxa 9:238–253.
8. Desiro A, Duckett JG, Pressel S, Villarreal JC, Bidartondo MI (2013) Fungal symbioses in hornworts: A chequered history. Proc Biol Sci 280:20130207.
9. Wang B, et al. (2010) Presence of three mycorrhizal genes in the common ancestor of land plants suggests a key role of mycorrhizas in the colonization of land by plants. New Phytol 186:514–525.
10. Delaux P-M, et al. (2015) Algal ancestor of land plants was preadapted for symbiosis. Proc Natl Acad Sci USA 112:13390–13395.
11. Petre B, Kamoun S (2014) How do filamentous pathogens deliver effector proteins into plant cells? PLoS Biol 12:e1001801.
12. Roth R, Paszkowski U (2017) Plant carbon nourishment of arbuscular mycorrhizal fungi. Curr Opin Plant Biol 39:50–56.
13. Parniske M (2000) Intracellular accommodation of microbes by plants: a common developmental program for symbiosis and disease? Curr Opin Plant Biol 3:320–328.
14. Rey T, Schornack S (2013) Interactions of beneficial and detrimental root-colonizing filamentous microbes with plant hosts. Genome Biol 14:121.
15. Ivanov S, Fedorova E, Bisseling T (2010) Intracellular plant microbe associations: secretory pathways and the formation of perimicrobial compartments. Curr Opin Plant Biol 13:372–377.
16. Zeilinger S, et al. (2016) Friends or foes? Emerging insights from fungal interactions with plants. FEMS Microbiol Rev 40:182–207.
17. Carella P, Schornack S (2017) Manipulation of bryophyte hosts by pathogenic and symbiotic microbes. Plant Cell Physiol, 10.1093/pcp/pcx182.
18. Qiu YL, et al. (2006) The deepest divergences in land plants inferred from phyloge-nomic evidence. Proc Natl Acad Sci USA 103:15511–15516.
19. Renzaglia KS, et al. (2007) Bryophyte phylogeny: Advancing the molecular and morphological frontiers. Bryologist 110:179–213.
20. Cox CJ, Li B, Foster PG, Embley TM, Civán P (2014) Conflicting phylogenies for early land plants are caused by composition biases among synonymous substitutions. Syst Biol 63:272–279.
21. Ruhfel BR, Gitzendanner MA, Soltis PS, Soltis DE, Burleigh JG (2014) From algae to angiosperms-inferring the phylogeny of green plants (Viridiplantae) from 360 plastid genomes. BMC Evol Biol 14:23.
22. Ponce de León I (2011) The moss Physcomitrella patens as a model system to study interactions between plants and phytopathogenic fungi and oomycetes. J Pathogens 2011:719873.
23. Overdijk EJ, et al. (2016) Interaction between the moss Physcomitrella patens and Phytophthora: a novel pathosystem for live-cell imaging of subcellular defence. J Microsc 263:171–180.
24. Ponce de León I, Montesano M (2017) Adaptation mechanisms in the evolution of moss defenses to microbes. Front Plant Sci 8:366.
25. Ishizaki K, Nishihama R, Yamato KT, Kohchi T (2016) Molecular genetic tools and techniques for Marchantia polymorpha research. Plant Cell Physiol 57:262–270.
26. Shimamura M (2016) Marchantia polymorpha: Taxonomy, phylogeny, and morphology of a model system. Plant Cell Physiol 57:230–256.
27. Rey T, Chatterjee A, Buttay M, Toulotte J, Schornack S (2015) Medicago truncatula symbiosis mutants affected in the interaction with a biotrophic root pathogen. New Phytol 206:497–500.
28. Le Fevre R, O’Boyle B, Moscou MJ, Schornack S (2016) Colonization of barley by the broad-host hemibiotrophic pathogen Phytophthora palmivora uncovers a leaf development-dependent involvement of Mlo. Mol Plant Microbe Interact 29:385–395.
29. Evangelisti E, et al. (2017) Time-resolved dual root-microbe transcriptomics reveals early induced Nicotiana benthamiana genes and conserved infection-promoting Phytophthora palmivora effectors. BMC Biol 15:39.
30. Judelson HS, Blanco FA (2005) The spores of Phytophthora: weapons of the plant destroyer. Nat Rev Microbiol 3:47–58.
31. Morgan W, Kamoun S (2007) RXLR effectors of plant pathogenic oomycetes. Curr Opin Microbiol 10:332–338.
32. Anderson RG, Deb D, Fedkenheuer K, McDowell JM (2015) Recent progress in RXLR effector research. Mol Plant Microbe Interact 28:1063–1072.
33. Wang S, et al. (2017) Delivery of cytoplasmic and apoplastic effectors from Phytophthora infestans haustoria by distinct secretion pathways. New Phytol 216: 205–215.
34. Hardham AR (2007) Cell biology of plant-oomycete interactions. Cell Microbiol 9: 31–39.
35. Torres GA, et al. (2016) Bud rot caused by Phytophthora palmivora: A destructive emerging disease of oil palm. Phytopathology 106:320–329.
36. Boller T, Felix G (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60:379–406.
37. Lehtonen MT, et al. (2009) Quickly-released peroxidase of moss in defense against fungal invaders. New Phytol 183:432–443.
38. Ponce De León I, et al. (2012) Physcomitrella patens activates reinforcement of the cell wall, programmed cell death and accumulation of evolutionary conserved defence signals, such as salicylic acid and 12-oxo-phytodienoic acid, but not jasmonic acid, upon Botrytis cinerea infection. Mol Plant Pathol 13:960–974.
39. Avrova AO, et al. (2008) A novel Phytophthora infestans haustorium-specific membrane protein is required for infection of potato. Cell Microbiol 10:2271–2284.
40. Ah Fong AMV, Judelson HS (2003) Cell cycle regulator Cdc14 is expressed during sporulation but not hyphal growth in the fungus-like oomycete Phytophthora infestans. Mol Microbiol 50:487–494.
41. Wang Q, et al. (2011) Transcriptional programming and functional interactions within the Phytophthora sojae RXLR effector repertoire. Plant Cell 23:2064–2086.
42. Jupe J, et al. (2013) Phytophthora capsici-tomato interaction features dramatic shifts in gene expression associated with a hemi-biotrophic lifestyle. Genome Biol 14:R63.
43. Haas BJ, et al. (2009) Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461:393–398.
44. Bellincampi D, Cervone F, Lionetti V (2014) Plant cell wall dynamics and wall-related susceptibility in plant-pathogen interactions. Front Plant Sci 5:228.
45. Faulkner C (2015) A cellular backline: specialization of host membranes for defence. J Exp Bot 66:1565–1571.
46. Bozkurt TO, et al. (2015) Rerouting of plant late endocytic trafficking toward a pathogen interface. Traffic 16:204–226.
47. Lu YJ, et al. (2012) Patterns of plant subcellular responses to successful oomycete infections reveal differences in host cell reprogramming and endocytic trafficking. Cell Microbiol 14:682–697.
48. Zhang C, Hicks GR, Raikhel NV (2014) Plant vacuole morphology and vacuolar trafficking. Front Plant Sci 5:476.
49. Bowman JL, et al. (2017) Insights into land plant evolution garnered from the Marchantia polymorpha genome. Cell 171:287–304.e15.
50. Gu Y, Zavaliev R, Dong X (2017) Membrane trafficking in plant immunity. Mol Plant 10:1026–1034.
51. Kanazawa T, Ueda T (2017) Exocytic trafficking pathways in plants: why and how they are redirected. New Phytol 215:952–957.
52. Kanazawa T, et al. (2016) SNARE molecules in Marchantia polymorpha: Unique and conserved features of the membrane fusion machinery. Plant Cell Physiol 57:307–324.
53. Ishizaki K, et al. (2013) Essential role of the E3 ubiquitin ligase nopperabo1 in schizogenous intercellular space formation in the liverwort Marchantia polymorpha. Plant Cell 25:4075–4084.
54. Bozkurt TO, et al. (2014) The plant membrane-associated REMORIN1.3 accumulates in discrete perihaustorial domains and enhances susceptibility to Phytophthora infestans. Plant Physiol 165:1005–1018.
55. Pan H, et al. (2016) A symbiotic SNARE protein generated by alternative termination of transcription. Nat Plants 2:15197.
56. Schussler A (2000) Glomus claroideum forms an arbuscular mycorrhiza-like symbiosis with the hornwort Anthoceros punctatus. Mycorrhiza 10:15–21.
57. McLachlan DH, Kopischke M, Robatzek S (2014) Gate control: guard cell regulation by microbial stress. New Phytol 203:1049–1063.
58. Melotto M, Zhang L, Oblessuc PR, He S-Y (2017) Stomatal defense a decade later. Plant Physiol 174:561–571.
59. Field KJ, Duckett JG, Cameron DD, Pressel S (2015) Stomatal density and aperture in non-vascular land plants are non-responsive to above-ambient atmospheric CO2 concentrations. Ann Bot 115:915–922.
60. Sarkar P, Bosneaga E, Auer M (2009) Plant cell walls throughout evolution: towards a molecular understanding of their design principles. J Exp Bot 60:3615–3635.
61. Takikawa Y, et al. (2014) Targeted destruction of fungal structures of Erysiphe trifoliorum on flat leaf surfaces of Marchantia polymorpha. Plant Biol (Stuttg) 16: 291–295.
62. Latijnhouwers M, de Wit PJGM, Govers F (2003) Oomycetes and fungi: similar weaponry to attack plants. Trends Microbiol 11:462–469.
63. Wang E, et al. (2012) A common signaling process that promotes mycorrhizal and oomycete colonization of plants. Curr Biol 22:2242–2246.
64. Ligrone R, Duckett JG, Renzaglia KS (2012) Major transitions in the evolution of early land plants: a bryological perspective. Ann Bot 109:851–871.
65. Solomon PS, Oliver RP (2002) Evidence that gamma-aminobutyric acid is a major nitrogen source during Cladosporium fulvum infection of tomato. Planta 214:414–420.
66. de Wit PJ (2016) Cladosporium fulvum effectors: Weapons in the arms race with tomato. Annu Rev Phytopathol 54:1–23.
67. Catalano CM, Czymmek KJ, Gann JG, Sherrier DJ (2007) Medicago truncatula syntaxin SYP132 defines the symbiosome membrane and infection droplet membrane in root nodules. Planta 225:541–550.
68. Caillaud M-C, et al. (2014) The plasmodesmal protein PDLP1 localises to haustoria-associated membranes during downy mildew infection and regulates callose deposition. PLoS Pathog 10:e1004496.
69. Wightman R, Wallis S, Aston P (2017) Hydathode pit development in the alpine plant Saxifraga cochlearis. Flora 233:99–108.
70. Koressaar T, Remm M (2007) Enhancements and modifications of primer design program Primer3. Bioinformatics 23:1289–1291.
71. Untergasser A, et al. (2012) Primer3—new capabilities and interfaces. Nucleic Acids Res 40:e115.
72. Ishizaki K, et al. (2015) Development of gateway binary vector series with four different selection markers for the liverwort Marchantia polymorpha. PLoS One 10: e0138876.
73. Kubota A, Ishizaki K, Hosaka M, Kohchi T (2013) Efficient Agrobacterium-mediated transformation of the liverwort Marchantia polymorpha using regenerating thalli. Biosci Biotechnol Biochem 77:167–172.
74. Ali SS, et al. (2017) Phytophthora megakarya and P. palmivora, closely related causal agents of cacao black pod rot, underwent increases in genome sizes and gene numbers by different mechanisms. Genome Biol Evol 9:536–557.
75. Liao Y, Smyth GK, Shi W (2014) featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30:923–930.
76. Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:550.
77. Kolde R (2015) Package “pheatmap”: Pretty heatmaps. R package, version 1.0.8. Available at https://cran.r-project.org/web/packages/pheatmap/pheatmap.pdf. Accessed April 1, 2017.
78. Gogleva A, Drost H-G, Schornack S (2018) SecretSanta: flexible pipelines for functional secretome prediction. Bioinformatics 10.1093/bioinformatics/bty088.