Abstract
Arabidopsis thaliana exhibits a durable resistance called nonhost resistance against nonadapted fungal pathogens. A. thaliana activates preinvasive resistance and terminates entry attempts by nonadapted fungi belonging to the genus Colletotrichum, which cause anthracnose disease in many plants. In the interaction between A. thaliana and nonadapted C. tropicale, the preinvasive resistance involves the PENETRATION 2-related antifungal secondary metabolite pathway and the ENHANCED DISEASE RESISTANCE 1-dependent antifungal peptide pathway. The development of invasive hyphae by C. tropicale owing to the reduction of preinvasive resistance then triggers the blockage of further hyphal expansion via the activation of the second layer of resistance, i.e., postinvasive resistance, which guarantees the robustness of the nonhost resistance of A. thaliana against Colletotrichum pathogens. Both the tryptophan-derived metabolic pathway and glutathione synthesis play critical roles in the postinvasive resistance against C. tropicale, although the molecular mechanism of postinvasive resistance remains to be elucidated. In this review, we describe the current understanding of the molecular background of the Arabidopsis nonhost resistance against Colletotrichum fungi and discuss perspectives for future research on this durable resistance.
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References
Agrios GN (2004) Plant pathology, 5th edn. Elsevier Academic Press, San Diego
Anderson JP, Badruzsaufari E, Schenk PM, Manners JM, Desmond OJ, Ehlert C, Maclean DJ, Ebert PR, Kazan K (2004) Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. Plant Cell 16:3460–3479
Assaad FF, Qiu JL, Youngs H, Ehrhardt D, Zimmerli L, Kalde M, Wanner G, Peck SC, Edwards H, Ramonell K, Somerville CR, Thordal-Christensen H (2004) The PEN1 syntaxin defines a novel cellular compartment upon fungal attack and is required for the timely assembly of papillae. Mol Biol Cell 15:5118–5129
Bednarek P (2012) Sulfur-containing secondary metabolites from Arabidopsis thaliana and other Brassicaceae with function in plant immunity. Chem Bio Chem 13:1846–1859
Bednarek P, Piślewska-Bednarek M, Svatos A, Schneider B, Doubsky J, Mansurova M, Humphry M, Consonni C, Panstruga R, Sanchez-Vallet A, Molina A, Schulze-Lefert P (2009) A glucosinolate metabolism pathway in living plant cells mediates broad-spectrum antifungal defense. Science 323:101–106
Bhat RA, Miklis M, Schmelzer E, Schulze-Lefert P, Panstruga R (2005) Recruitment and interaction dynamics of plant penetration resistance components in a plasma membrane microdomain. Proc Natl Acad Sci USA 102:3135–3140
Birker D, Heidrich K, Takahara H, Narusaka M, Deslandes L, Narusaka Y, Reymond M, Parker JE, O’Connell R (2009) A locus conferring resistance to Colletotrichum higginsianum is shared by four geographically distinct Arabidopsis accessions. Plant J 60:602–613
Böttcher C, Westphal L, Schmotz C, Prade E, Scheel D, Glawischnig E (2009) The multifunctional enzyme CYP71B15 (PHYTOALEXIN DEFICIENT3) converts cysteine-indole-3-acetonitrile to camalexin in the indole-3-acetonitrile metabolic network of Arabidopsis thaliana. Plant Cell 21:1830–1845
Clay NK, Adio AM, Denoux C, Jander G, Ausubel FM (2009) Glucosinolate metabolites required for an Arabidopsis innate immune response. Science 323:95–101
Collins NC, Thordal-Christensen H, Lipka V, Bau S, Kombrink E, Qiu JL, Huckelhoven R, Stein M, Freialdenhoven A, Somerville SC, Schulze-Lefert P (2003) SNARE-protein-mediated disease resistance at the plant cell wall. Nature 425:973–977
Frye CA, Innes RW (1998) An Arabidopsis mutant with enhanced resistance to powdery mildew. Plant Cell 10:947–956
Frye CA, Tang D, Innes RW (2001) Negative regulation of defense responses in plants by a conserved MAPKK kinase. Proc Natl Acad Sci USA 98:373–378
Fuchs R, Kopischke M, Klapprodt C, Hause G, Meyer AJ, Schwarzländer M, Fricker MD, Lipka V (2016) Immobilized subpopulations of leaf epidermal mitochondria mediate PENETRATION2-dependent pathogen entry control in Arabidopsis. Plant Cell 28:130–145
Fukunaga S, Sogame M, Hata M, Singkaravanit-Ogawa S, Piślewska-Bednarek M, Onozawa-Komori M, Nishiuchi T, Hiruma K, Saitoh H, Terauchi R, Kitakura S, Inoue Y, Bednarek P, Schulze-Lefert P, Takano Y (2017) Dysfunction of Arabidopsis MACPF domain protein activates programmed cell death via tryptophan metabolism in MAMP-triggered immunity. Plant J 89:381–393
Glazebrook J, Ausubel FM (1994) Isolation of phytoalexin-deficient mutants of Arabidopsis thaliana and characterization of their interactions with bacterial pathogens. Proc Natl Acad Sci USA 91:8955–8959
Heath MC (2000) Nonhost resistance and nonspecific plant defenses. Curr Opin Plant Biol 3:315–319
Hiruma K, Takano Y (2010) Roles of EDR1 in non-host resistance of Arabidopsis. Plant Signal Behav 6:1831–1833
Hiruma K, Onozawa-Komori M, Takahashi F, Asakura M, Bednarek P, Okuno T, Schulze-Lefert P, Takano Y (2010) Entry mode-dependent function of an indole glucosinolate pathway in Arabidopsis for nonhost resistance against anthracnose pathogens. Plant Cell 22:2429–2443
Hiruma K, Nishiuchi T, Kato T, Bednarek P, Okuno T, Schulze-Lefert P, Takano Y (2011) Arabidopsis ENHANCED DISEASE RESISTANCE 1 is required for pathogen-induced expression of plant defensins in nonhost resistance, and acts through interference of MYC2-mediated repressor function. Plant J 67:980–992
Hiruma K, Fukunaga S, Bednarek P, Piślewska-Bednarek M, Watanabe S, Narusaka Y, Shirasu K, Takano Y (2013) Glutathione and tryptophan metabolism are required for Arabidopsis immunity during the hypersensitive response to hemibiotrophs. PNAS 110:9589–9594
Jacobs A, Lipka V, Burton R, Panstruga R, Strizhov N, Schulze-Lefert P, Fincher G (2003) An Arabidopsis callose synthase, GSL5, is required for wound and papillary callose formation. Plant Cell 15:2503–2513
Johansson ON, Fantozzi E, Fahlberg P, Nilsson AK, Buhot N, Tör M, Andersson MX (2014) Role of the penetration-resistance genes PEN1, PEN2 and PEN3 in the hypersensitive response and race-specific resistance in Arabidopsis thaliana. Plant J 79:466–476
Kobayashi I, Kobayashi Y, Yamaoka N, Kunoh H (1992) Recognition of a pathogen and a nonpathogen by barley coleoptile cells. III. Responses of microtubules and actin filaments in barley coleoptile cells to penetration attempts. Can J Bot 70:1815–1823
Kojima K, Kikuchi T, Takano Y, Oshiro E, Okuno T (2002) The mitogen-activated protein kinase gene MAF1 is essential for the early differentiation phase of appressorium formation in Colletotrichum lagenarium. Mol Plant Microbe Interact 15:1268–1276
Kubo Y, Furusawa I (1991) Melanin biosynthesis: prerequisite for successful invasion of the plant host by appressoria of Colletotrichum and Pyricularia. In: Cole GT, Hoch HC (eds) The fungal spore and disease initiation in plants and animals. Plenum, New York, pp 205–217
Kubo Y, Takano Y (2013) Dynamics of infection-related morphogenesis and pathogenesis in Colletotrichum orbiculare. J Gen Plant Pathol 79:233–242
Kwon C, Neu C, Pajonk S, Yun HS, Lipka U, Humphry M, Bau S, Straus M, Kwaaitaal M, Rampelt H, El Kasmi F, Jürgens G, Parker J, Panstruga R, Lipka V, Schulze-Lefert P (2008) Co-option of a default secretory pathway for plant immune responses. Nature 451:835–840
Lipka V, Dittgen J, Bednarek P, Bhat R, Wiermer M, Stein M, Landtag J, Brandt W, Rosahl S, Scheel D, Llorente F, Molina A, Parker J, Somerville S, Schulze-Lefert P (2005) Pre- and postinvasion defenses both contribute to nonhost resistance in Arabidopsis. Science 310:1180–1183
Lipka U, Fuchs R, Lipka V (2008) Arabidopsis nonhost resistance to powdery mildews. Curr Opin Plant Biol 11:404–411
Lorenzo O, Chico JM, Sanchez-Serrano JJ, Solano R (2004) JASMONATE-INSENSITIVE1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defense responses in Arabidopsis. Plant Cell 16:1938–1950
Matsushima R, Hayashi Y, Yamada K, Shimada T, Nishimura M, Hara-Nishimura I (2003) The ER body, a novel endoplasmic reticulum-derived structure in Arabidopsis. Plant Cell Physiol 44:661–666
Mélida H, Sopeña-Torres S, Bacete L, Garrido-Arandia M, Jordá L, López G, Muñoz-Barrios A, Pacios LF, Molina A (2018) Non-branched β-1,3-glucan oligosaccharides trigger immune responses in Arabidopsis. Plant J 93:34–49
Miya A, Albert P, Shinya T, Desaki Y, Ichimura K, Shirasu K, Narusaka Y, Kawakami N, Kaku H, Shibuya N (2007) CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc Natl Acad Sci USA 104:19613–19618
Narusaka Y, Narusaka M, Park P, Kubo Y, Hirayama T, Seki M, Shiraishi T, Ishida J, Nakashima M, Enju A, Sakurai T, Satou M, Kobayashi M, Shinozaki K (2004) RCH1, a locus in Arabidopsis that confers resistance to the hemibiotrophic fungal pathogen Colletotrichum higginsianum. Mol Plant Microbe Interact 17:749–762
Narusaka M, Shirasu K, Noutoshi Y, Kubo Y, Shiraishi T, Iwabuchi M, Narusaka Y (2009) RRS1 and RPS4 provide a dual resistance-gene system against fungal and bacterial pathogens. Plant J 60:218–226
Nishimura M, Stein M, Hou B, Vogel J, Edwards H, Somerville S (2003) Loss of a callose synthase results in salicylic acid-dependent disease resistance. Science 301:969–972
Noutoshi Y, Kuromori T, Wada T, Hirayama T, Kamiya A, Imura Y, Yasuda M, Nakashita H, Shirasu K, Shinozaki K (2006) Loss of Necrotic Spotted Lesions 1 associates with cell death and defense responses in Arabidopsis thaliana. Plant Mol Biol 62:29–42
Nürnberger T, Lipka V (2005) Non-host resistance in plants: new insights into an old phenomenon. Mol Plant Pathol 6:335–345
O’Connell R, Herbert C, Sreenivasaprasad S, Khatib M, Esquerré -Tugayé M, Dumas B (2004) A novel Arabidopsis–Colletotrichum pathosystem for the molecular dissection of plant fungal interactions. Mol Plant Microbe Interact 17:272–282
Parisy V, Poinssot B, Owsianowski L, Buchala A, Glazebrook J, Mauch F (2007) Identification of PAD2 as a γ-glutamylcysteine synthetase highlights the importance of glutathione in disease resistance of Arabidopsis. Plant J 49:157–172
Perfect SE, Hughes HB, O’Connell RJ, Green JR (1999) Colletotrichum: a model genus for studies on pathology and fungal–plant interactions. Fungal Genet Biol 27:186–198
Roetschi A, Si-Ammour A, Belbahri L, Mauch F, Mauch-Mani B (2001) Characterization of an Arabidopsis–Phytophthora pathosystem: resistance requires a functional PAD2 gene and is independent of salicylic acid, ethylene and jasmonic acid signalling. Plant J 28:293–305
Sanchez-Vallet A, Ramos B, Bednarek P, López G, Piślewska-Bednarek M, Schulze-Lefert P, Molina A (2010) Tryptophan-derived secondary metabolites in Arabidopsis thaliana confer non-host resistance to necrotrophic Plectosphaerella cucumerina fungi. Plant J 63:115–127
Schlaeppi K, Abou-Mansour E, Buchala A, Mauch F (2010) Disease resistance of Arabidopsis to Phytophthora brassicae is established by the sequential action of indole glucosinolates and camalexin. Plant J 62:840–851
Sels J, Mathys J, De Coninck BM, Cammue BP, De Bolle MF (2008) Plant pathogenesis-related (PR) proteins: a focus on PR peptides. Plant Physiol Biochem 46:941–950
Shimada C, Lipka V, O’Connell R, Okuno T, Schulze-Lefert P, Takano Y (2006) Nonhost resistance in Arabidopsis-Colletotrichum interactions acts at the cell periphery and requires actin filament function. Mol Plant Microbe Interact 19:270–279
Stein M, Dittgen J, Sánchez-Rodríguez C, Hou BH, Molina A, Schulze-Lefert P, Lipka V, Somerville S (2006) Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to nonhost resistance to inappropriate pathogens that enter by direct penetration. Plant Cell 18:731–746
Thomma BP, Cammue BP, Thevissen K (2002) Plant defensins. Planta 216:193–202
Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB (1997) Subcellular localization of H2O2 in plants, H2O2 accumulation in papillae and hypersensitive response during barley-powdery mildew interaction. Plant J 11:1187–1194
Wan J, Zhang XC, Neece D, Ramonell KM, Clough S, Kim SY, Stacey MG, Stacey G (2008) A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. Plant Cell 20:471–481
Watanabe S, Shimada TL, Hiruma K, Takano Y (2013) Pathogen infection trial increases the secretion of proteins localized in the endoplasmic reticulum body of Arabidopsis. Plant Physiol 163:659–664
Yun HP, Kang BG, Kwon C (2016) Arabidopsis immune secretory pathways to powdery mildew fungi. Plant Signal Behav 11:10 e1226456
Zhao Y, Hull AK, Gupta NR, Goss KA, Alonso J, Ecker JR, Normanly J, Chory J, Celenza JL (2002) Trp-dependent auxin biosynthesis in Arabidopsis: involvement of cytochrome P450s CYP79B2 and CYP79B3. Genes Dev 16:3100–3112
Zhou N, Tootle TL, Glazebrook J (1999) Arabidopsis PAD3, a gene required for camalexin biosynthesis, encodes a putative cytochrome P450 monooxygenase. Plant Cell 11:2419–2428
Acknowledgements
This work was supported in part by Grants-in-Aid for Scientific Research (KAKENHI) (15H05780, 18H02204 and 18H04780), by grants from the Project of the NARO Bio-oriented Technology Research Advancement Institution (research program on development of innovative technology), and by the Asahi Glass Foundation.
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Kosaka, A., Takano, Y. Nonhost resistance of Arabidopsis thaliana against Colletotrichum species. J Gen Plant Pathol 84, 305–311 (2018). https://doi.org/10.1007/s10327-018-0799-y
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DOI: https://doi.org/10.1007/s10327-018-0799-y