Conserved Biochemical Defenses Underpin Host Responses to Oomycete Infection in an Early-Divergent Land Plant Lineage

Current Biology

Volumn 29, Issue 14, 2019, Pages 2282-2294.e5

  Carella, Philip ^a   Gogleva, Anna ^a   Hoey, David John ^a   Bridgen, Anthony John ^a   Stolze, Sara Christina ^b   Nakagami, Hirofumi ^b   Schornack, Sebastian ^a,c  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

bryophyte; evolution; flavonoid; liverwort; Marchantia; Nicotiana; oomycete; phenylpropanoid; Phytophthora; R2R3 MYB

Indexed keywords

EVOLUTION; HOST PATHOGEN INTERACTION; IMMUNOLOGY; MARCHANTIA; MICROBIOLOGY; PHYSIOLOGY; PHYTOPHTHORA; PLANT DISEASE; PLANT GENE; PLANT IMMUNITY; TOBACCO;

BIOLOGICAL EVOLUTION; GENES, PLANT; HOST-PATHOGEN INTERACTIONS; MARCHANTIA; PHYTOPHTHORA; PLANT DISEASES; PLANT IMMUNITY; TOBACCO;

EID: 85069054385     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2019.05.078     Document Type: Article

References (84)

1. Remy, W., Taylor, T.N., Hass, H., Kerp, H., Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proc. Natl. Acad. Sci. USA 91 (1994), 11841–11843.
2. Taylor, T.N., Remy, W., Hass, H., Kerp, H., Fossil arbuscular mycorrhizae from the Early Devonian. Mycologia 87 (1995), 560–573.
3. Taylor, T.N., Krings, M., Kerp, H., Hassiella monospora gen. et sp. nov., a microfungus from the 400 million year old Rhynie chert. Mycol. Res. 110 (2006), 628–632.
4. Strullu-Derrien, C., Fossil filamentous microorganisms associated with plants in early terrestrial environments. Curr. Opin. Plant Biol. 44 (2018), 122–128.
5. Krings, M., Taylor, T.N., Hass, H., Kerp, H., Dotzler, N., Hermsen, E.J., Fungal endophytes in a 400-million-yr-old land plant: infection pathways, spatial distribution, and host responses. New Phytol. 174 (2007), 648–657.
6. Boller, T., Felix, G., A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu. Rev. Plant Biol. 60 (2009), 379–406.
7. Macho, A.P., Zipfel, C., Plant PRRs and the activation of innate immune signaling. Mol. Cell 54 (2014), 263–272.
8. Cui, H., Tsuda, K., Parker, J.E., Effector-triggered immunity: from pathogen perception to robust defense. Annu. Rev. Plant Biol. 66 (2015), 487–511.
9. Bednarek, P., Chemical warfare or modulators of defence responses—the function of secondary metabolites in plant immunity. Curr. Opin. Plant Biol. 15 (2012), 407–414.
10. Meng, X., Zhang, S., MAPK cascades in plant disease resistance signaling. Annu. Rev. Phytopathol. 51 (2013), 245–266.
11. Morris, J.L., Puttick, M.N., Clark, J.W., Edwards, D., Kenrick, P., Pressel, S., Wellman, C.H., Yang, Z., Schneider, H., Donoghue, P.C.J., The timescale of early land plant evolution. Proc. Natl. Acad. Sci. USA 115 (2018), E2274–E2283.
12. 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., Donoghue, P.C.J., The interrelationships of land plants and the nature of the ancestral embryophyte. Curr. Biol. 28 (2018), 733–745.e2.
13. de Sousa, F., Foster, P.G., Donoghue, P.C.J., Schneider, H., Cox, C.J., Nuclear protein phylogenies support the monophyly of the three bryophyte groups (Bryophyta Schimp.). New Phytol. 222 (2019), 565–575.
14. Rensing, S.A., Lang, D., Zimmer, A.D., Terry, A., Salamov, A., Shapiro, H., Nishiyama, T., Perroud, P.-F., Lindquist, E.A., Kamisugi, Y., et al. The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319 (2008), 64–69.
15. Bowman, J.L., Kohchi, T., Yamato, K.T., Jenkins, J., Shu, S., Ishizaki, K., Yamaoka, S., Nishihama, R., Nakamura, Y., Berger, F., et al. Insights into land plant evolution garnered from the Marchantia polymorpha genome. Cell 171 (2017), 287–304.e15.
16. Ponce de León, I., Montesano, M., Adaptation mechanisms in the evolution of moss defenses to microbes. Front. Plant Sci., 8, 2017, 366.
17. Carella, P., Schornack, S., Manipulation of bryophyte hosts by pathogenic and symbiotic microbes. Plant Cell Physiol. 59 (2018), 651–660.
18. de Vries, S., de Vries, J., von Dahlen, J.K., Gould, S.B., Archibald, J.M., Rose, L.E., Slamovits, C.H., On plant defense signaling networks and early land plant evolution. Commun. Integr. Biol. 11 (2018), 1–14.
19. 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. Algal ancestor of land plants was preadapted for symbiosis. Proc. Natl. Acad. Sci. USA 112 (2015), 13390–13395.
20. Field, K.J., Pressel, S., Unity in diversity: structural and functional insights into the ancient partnerships between plants and fungi. New Phytol. 220 (2018), 996–1011.
21. Bressendorff, S., Azevedo, R., Kenchappa, C.S., Ponce de León, I., Olsen, J.V., Rasmussen, M.W., Erbs, G., Newman, M.-A., Petersen, M., Mundy, J., An innate immunity pathway in the moss Physcomitrella patens. Plant Cell 28 (2016), 1328–1342.
22. Reboledo, G., Del Campo, R., Alvarez, A., Montesano, M., Mara, H., Ponce de León, I., Physcomitrella patens activates defense responses against the pathogen Colletotrichum gloeosporioides. Int. J. Mol. Sci. 16 (2015), 22280–22298.
23. Overdijk, E.J.R., De Keijzer, J., De Groot, D., Schoina, C., Bouwmeester, K., Ketelaar, T., Govers, F., Interaction between the moss Physcomitrella patens and Phytophthora: a novel pathosystem for live-cell imaging of subcellular defence. J. Microsc. 263 (2016), 171–180.
24. Monte, I., Ishida, S., Zamarreño, A.M., Hamberg, M., Franco-Zorrilla, J.M., García-Casado, G., Gouhier-Darimont, C., Reymond, P., Takahashi, K., García-Mina, J.M., et al. Ligand-receptor co-evolution shaped the jasmonate pathway in land plants. Nat. Chem. Biol. 14 (2018), 480–488.
25. Nelson, J.M., Hauser, D.A., Hinson, R., Shaw, A.J., A novel experimental system using the liverwort Marchantia polymorpha and its fungal endophytes reveals diverse and context-dependent effects. New Phytol. 218 (2018), 1217–1232.
26. Carella, P., Gogleva, A., Tomaselli, M., Alfs, C., Schornack, S., Phytophthora palmivora establishes tissue-specific intracellular infection structures in the earliest divergent land plant lineage. Proc. Natl. Acad. Sci. USA 115 (2018), E3846–E3855.
27. van Loon, L.C., Pierpoint, W.S., Boller, Th., Conejero, V., Recommendations for naming plant pathogenesis-related proteins. Plant Mol. Biol. Report. 12 (1994), 245–264.
28. Sels, J., Mathys, J., De Coninck, B.M.A., Cammue, B.P.A., De Bolle, M.F.C., Plant pathogenesis-related (PR) proteins: a focus on PR peptides. Plant Physiol. Biochem. 46 (2008), 941–950.
29. Ali, S., Ganai, B.A., Kamili, A.N., Bhat, A.A., Mir, Z.A., Bhat, J.A., Tyagi, A., Islam, S.T., Mushtaq, M., Yadav, P., et al. Pathogenesis-related proteins and peptides as promising tools for engineering plants with multiple stress tolerance. Microbiol. Res. 212–213 (2018), 29–37.
30. Visser, E.A., Wegrzyn, J.L., Myburg, A.A., Naidoo, S., Defence transcriptome assembly and pathogenesis related gene family analysis in Pinus tecunumanii (low elevation). BMC Genomics, 19, 2018, 632.
31. Evangelisti, E., Gogleva, A., Hainaux, T., Doumane, M., Tulin, F., Quan, C., Yunusov, T., Floch, K., Schornack, S., Time-resolved dual transcriptomics reveal early induced Nicotiana benthamiana root genes and conserved infection-promoting Phytophthora palmivora effectors. BMC Biol., 15, 2017, 39.
32. Emms, D.M., Kelly, S., OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol., 16, 2015, 157.
33. Liu, J., Osbourn, A., Ma, P., MYB transcription factors as regulators of phenylpropanoid metabolism in plants. Mol. Plant 8 (2015), 689–708.
34. Xu, W., Dubos, C., Lepiniec, L., Transcriptional control of flavonoid biosynthesis by MYB-bHLH-WDR complexes. Trends Plant Sci. 20 (2015), 176–185.
35. Albert, N.W., Thrimawithana, A.H., McGhie, T.K., Clayton, W.A., Deroles, S.C., Schwinn, K.E., Bowman, J.L., Jordan, B.R., Davies, K.M., Genetic analysis of the liverwort Marchantia polymorpha reveals that R2R3MYB activation of flavonoid production in response to abiotic stress is an ancient character in land plants. New Phytol. 218 (2018), 554–566.
36. Clayton, W.A., Albert, N.W., Thrimawithana, A.H., McGhie, T.K., Deroles, S.C., Schwinn, K.E., Warren, B.A., McLachlan, A.R.G., Bowman, J.L., Jordan, B.R., Davies, K.M., UVR8-mediated induction of flavonoid biosynthesis for UVB tolerance is conserved between the liverwort Marchantia polymorpha and flowering plants. Plant J. 96 (2018), 503–517.
37. Kubo, H., Nozawa, S., Hiwatashi, T., Kondou, Y., Nakabayashi, R., Mori, T., Saito, K., Takanashi, K., Kohchi, T., Ishizaki, K., Biosynthesis of riccionidins and marchantins is regulated by R2R3-MYB transcription factors in Marchantia polymorpha. J. Plant Res. 131 (2018), 849–864.
38. Nishihama, R., Ishida, S., Urawa, H., Kamei, Y., Kohchi, T., Conditional gene expression/deletion systems for Marchantia polymorpha using its own heat-shock promoter and Cre/loxP-mediated site-specific recombination. Plant Cell Physiol. 57 (2016), 271–280.
39. Ishizaki, K., Nishihama, R., Ueda, M., Inoue, K., Ishida, S., Nishimura, Y., Shikanai, T., Kohchi, T., Development of Gateway binary vector series with four different selection markers for the liverwort Marchantia polymorpha. PLoS ONE, 10, 2015, e0138876.
40. Oliver, J.P., Castro, A., Gaggero, C., Cascón, T., Schmelz, E.A., Castresana, C., Ponce de León, I., Pythium infection activates conserved plant defense responses in mosses. Planta 230 (2009), 569–579.
41. Castro, A., Vidal, S., Ponce de León, I., Moss pathogenesis-related-10 protein enhances resistance to Pythium irregulare in Physcomitrella patens and Arabidopsis thaliana. Front. Plant Sci., 7, 2016, 580.
42. de Vries, S., de Vries, J., Teschke, H., von Dahlen, J.K., Rose, L.E., Gould, S.B., Jasmonic and salicylic acid response in the fern Azolla filiculoides and its cyanobiont. Plant Cell Environ. 41 (2018), 2530–2548.
43. Winter, P.S., Bowman, C.E., Villani, P.J., Dolan, T.E., Hauck, N.R., Systemic acquired resistance in moss: further evidence for conserved defense mechanisms in plants. PLoS ONE, 9, 2014, e101880.
44. Hirsch, S., Oldroyd, G.E.D., GRAS-domain transcription factors that regulate plant development. Plant Signal. Behav. 4 (2009), 698–700.
45. Grosche, C., Genau, A.C., Rensing, S.A., Evolution of the symbiosis-specific GRAS regulatory network in bryophytes. Front. Plant Sci., 9, 2018, 1621.
46. Rey, T., Bonhomme, M., Chatterjee, A., Gavrin, A., Toulotte, J., Yang, W., André, O., Jacquet, C., Schornack, S., The Medicago truncatula GRAS protein RAD1 supports arbuscular mycorrhiza symbiosis and Phytophthora palmivora susceptibility. J. Exp. Bot. 68 (2017), 5871–5881.
47. Vigneron, N., Radhakrishnan, G.V., Delaux, P.-M., What have we learnt from studying the evolution of the arbuscular mycorrhizal symbiosis?. Curr. Opin. Plant Biol. 44 (2018), 49–56.
48. Pandey, S.P., Somssich, I.E., The role of WRKY transcription factors in plant immunity. Plant Physiol. 150 (2009), 1648–1655.
49. Rushton, P.J., Somssich, I.E., Ringler, P., Shen, Q.J., WRKY transcription factors. Trends Plant Sci. 15 (2010), 247–258.
50. 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. A plant immune receptor detects pathogen effectors that target WRKY transcription factors. Cell 161 (2015), 1089–1100.
51. Sarris, P.F., Cevik, V., Dagdas, G., Jones, J.D.G., Krasileva, K.V., Comparative analysis of plant immune receptor architectures uncovers host proteins likely targeted by pathogens. BMC Biol., 14, 2016, 8.
52. Dixon, R.A., Achnine, L., Kota, P., Liu, C.-J., Reddy, M.S.S., Wang, L., The phenylpropanoid pathway and plant defence—a genomics perspective. Mol. Plant Pathol. 3 (2002), 371–390.
53. Naoumkina, M.A., Zhao, Q., Gallego-Giraldo, L., Dai, X., Zhao, P.X., Dixon, R.A., Genome-wide analysis of phenylpropanoid defence pathways. Mol. Plant Pathol. 11 (2010), 829–846.
54. Falcone Ferreyra, M.L., Rius, S.P., Casati, P., Flavonoids: biosynthesis, biological functions, and biotechnological applications. Front. Plant Sci., 3, 2012, 222.
55. Alvarez, A., Montesano, M., Schmelz, E., Ponce de León, I., Activation of shikimate, phenylpropanoid, oxylipins, and auxin pathways in Pectobacterium carotovorum elicitors-treated moss. Front. Plant Sci., 7, 2016, 328.
56. Cushnie, T.P.T., Lamb, A.J., Antimicrobial activity of flavonoids. Int. J. Antimicrob. Agents 26 (2005), 343–356.
57. Cisowska, A., Wojnicz, D., Hendrich, A.B., Anthocyanins as antimicrobial agents of natural plant origin. Nat. Prod. Commun. 6 (2011), 149–156.
58. Piasecka, A., Jedrzejczak-Rey, N., Bednarek, P., Secondary metabolites in plant innate immunity: conserved function of divergent chemicals. New Phytol. 206 (2015), 948–964.
59. Renault, H., Alber, A., Horst, N.A., Basilio Lopes, A., Fich, E.A., Kriegshauser, L., Wiedemann, G., Ullmann, P., Herrgott, L., Erhardt, M., et al. A phenol-enriched cuticle is ancestral to lignin evolution in land plants. Nat. Commun., 8, 2017, 14713.
60. Paniagua, C., Bilkova, A., Jackson, P., Dabravolski, S., Riber, W., Didi, V., Houser, J., Gigli-Bisceglia, N., Wimmerova, M., Budínská, E., et al. Dirigent proteins in plants: modulating cell wall metabolism during abiotic and biotic stress exposure. J. Exp. Bot. 68 (2017), 3287–3301.
61. Wu, Y.F., Zhao, Y., Liu, X.Y., Gao, S., Cheng, A.X., Lou, H.X., A bHLH transcription factor regulates bisbibenzyl biosynthesis in the liverwort Plagiochasma appendiculatum. Plant Cell Physiol. 59 (2018), 1187–1199.
62. Lillo, C., Lea, U.S., Ruoff, P., Nutrient depletion as a key factor for manipulating gene expression and product formation in different branches of the flavonoid pathway. Plant Cell Environ. 31 (2008), 587–601.
63. Shan, X., Zhang, Y., Peng, W., Wang, Z., Xie, D., Molecular mechanism for jasmonate-induction of anthocyanin accumulation in Arabidopsis. J. Exp. Bot. 60 (2009), 3849–3860.
64. Li, S., Wang, W., Gao, J., Yin, K., Wang, R., Wang, C., Petersen, M., Mundy, J., Qiu, J.-L., MYB75 phosphorylation by MPK4 is required for light-induced anthocyanin accumulation in Arabidopsis. Plant Cell 28 (2016), 2866–2883.
65. Wersch, R.V., Gao, F., Zhang, Y., Mitogen-activated protein kinase kinase 6 negatively regulates anthocyanin induction in Arabidopsis. Plant Signal. Behav., 13, 2018, e1526000.
66. Boter, M., Golz, J.F., Giménez-Ibañez, S., Fernandez-Barbero, G., Franco-Zorrilla, J.M., Solano, R., FILAMENTOUS FLOWER is a direct target of JAZ3 and modulates responses to jasmonate. Plant Cell 27 (2015), 3160–3174.
67. de Vries, J., de Vries, S., Slamovits, C.H., Rose, L.E., Archibald, J.M., How embryophytic is the biosynthesis of phenylpropanoids and their derivatives in streptophyte algae?. Plant Cell Physiol. 58 (2017), 934–945.
68. de Vries, J., Curtis, B.A., Gould, S.B., Archibald, J.M., Embryophyte stress signaling evolved in the algal progenitors of land plants. Proc. Natl. Acad. Sci. USA 115 (2018), E3471–E3480.
69. Tohge, T., Watanabe, M., Hoefgen, R., Fernie, A.R., The evolution of phenylpropanoid metabolism in the green lineage. Crit. Rev. Biochem. Mol. Biol. 48 (2013), 123–152.
70. Upson, J.L., Zess, E.K., Białas, A., Wu, C.H., Kamoun, S., The coming of age of EvoMPMI: evolutionary molecular plant-microbe interactions across multiple timescales. Curr. Opin. Plant Biol. 44 (2018), 108–116.
71. Ali, S.S., Shao, J., Lary, D.J., Kronmiller, B., Shen, D., Strem, M.D., Amoako-Attah, I., Akrofi, A.Y., Begoude, B.A.D., Ten Hoopen, G.M., et al. Phytophthora megakarya and Phytophthora 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 (2017), 536–557.
72. Le Fevre, R., O'Boyle, B., Moscou, M.J., Schornack, S., Colonization of barley by the broad-host hemibiotrophic pathogen Phytophthora palmivora uncovers a leaf development-dependent involvement of Mlo. Mol. Plant Microbe Interact. 29 (2016), 385–395.
73. Koressaar, T., Remm, M., Enhancements and modifications of primer design program Primer3. Bioinformatics 23 (2007), 1289–1291.
74. Untergasser, A., Cutcutache, I., Koressaar, T., Ye, J., Faircloth, B.C., Remm, M., Rozen, S.G., Primer3—new capabilities and interfaces. Nucleic Acids Res., 40, 2012, e115.
75. Cox, J., Mann, M., MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26 (2008), 1367–1372.
76. Tyanova, S., Temu, T., Cox, J., The MaxQuant computational platform for mass spectrometry-based shotgun proteomics. Nat. Protoc. 11 (2016), 2301–2319.
77. Love, M.I., Huber, W., Anders, S., Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol., 15, 2014, 550.
78. Dobin, A., Davis, C.A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S., Batut, P., Chaisson, M., Gingeras, T.R., STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29 (2013), 15–21.
79. Liao, Y., Smyth, G.K., Shi, W., featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30 (2014), 923–930.
80. Ah-Fong, A.M.V., Judelson, H.S., Vectors for fluorescent protein tagging in Phytophthora: tools for functional genomics and cell biology. Fungal Biol. 115 (2011), 882–890.
81. Rey, T., Chatterjee, A., Buttay, M., Toulotte, J., Schornack, S., Medicago truncatula symbiosis mutants affected in the interaction with a biotrophic root pathogen. New Phytol. 206 (2015), 497–500.
82. Saint-Marcoux, D., Proust, H., Dolan, L., Langdale, J.A., Identification of reference genes for real-time quantitative PCR experiments in the liverwort Marchantia polymorpha. PLoS ONE, 10, 2015, e0118678.
83. Borner, G.H.H., Fielding, A.B., Using in-solution digestion, peptide fractionation, and a Q Exactive mass spectrometer to analyze the proteome of clathrin-coated vesicles. Cold Spring Harb. Protoc. 2014 (2014), 1192–1195.
84. Kubota, A., Ishizaki, K., Hosaka, M., Kohchi, T., Efficient Agrobacterium-mediated transformation of the liverwort Marchantia polymorpha using regenerating thalli. Biosci. Biotechnol. Biochem. 77 (2013), 167–172.