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Rosette core fungal resistance in Arabidopsis thaliana

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Abstract

Main conclusion

Unlike rosette leaves, the mature Arabidopsis rosette core can display full resistance to Botrytis cinerea revealing the importance for spatial and developmental aspects of plant fungal resistance.

Abstract

Arabidopsis thaliana is a model host to investigate plant defense against fungi. However, many of the reports investigating Arabidopsis fungal defense against the necrotrophic fungus, Botrytis cinerea, utilize rosette leaves as host tissue. Here we report organ-dependent differences in B. cinerea resistance of Arabidopsis. Although wild-type Arabidopsis rosette leaves mount a jasmonate-dependent defense that slows fungal growth, this defense is incapable of resisting fungal devastation. In contrast, as the fungus spreads through infected leaf petioles towards the plant center, or rosette core, there is a jasmonate- and age-dependent fungal penetration blockage into the rosette core. We report evidence for induced and preformed resistance in the rosette core, as direct rosette core inoculation can also result in resistance, but at a lower penetrance relative to infections that approach the core from infected leaf petioles. The Arabidopsis rosette core displays a distinct transcriptome relative to other plant organs, and BLADE ON PETIOLE (BOP) transcripts are abundant in the rosette core. The BOP genes, with known roles in abscission zone formation, are required for full Arabidopsis rosette core B. cinerea resistance, suggesting a possible role for BOP-dependent modifications that may help to restrict fungal susceptibility of the rosette core. Finally, we demonstrate that cabbage and cauliflower, common Brassicaceae crops, also display leaf susceptibility and rosette core resistance to B. cinerea that can involve leaf abscission. Thus, spatial and developmental aspects of plant host resistance play critical roles in resistance to necrotrophic fungal pathogens and are important to our understanding of plant defense mechanisms.

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Abbreviations

BOP:

BLADE ON PETIOLE

MeJA:

Methyl jasmonate

JA-Ile:

Jasmonoyl-l-isoleucine

References

  • Browse J (2009) Jasmonate passes muster: a receptor and targets for the defense hormone. Annu Rev Plant Biol 60:183–205

    Article  CAS  PubMed  Google Scholar 

  • Buxdorf K, Yaffe H, Barda O, Levy M (2013) The effects of glucosinolates and their breakdown products on necrotrophic fungi. PLoS One 8:e70771

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chehab EW, Kaspi R, Savchenko T, Rowe H, Negre-Zakharov F, Kliebenstein D, Dehesh K (2008) Distinct roles of jasmonates and aldehydes in plant-defense responses. PLoS One 3:e1904

    Article  PubMed  PubMed Central  Google Scholar 

  • Chehab EW, Kim S, Savchenko T, Kliebenstein D, Dehesh K, Braam J (2011) Intronic T-DNA insertion renders Arabidopsis opr3 a conditional jasmonic acid-producing mutant. Plant Physiol 156:770–778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chini A, Monte I, Zamarreño AM, Hamberg M, Lassueur S, Reymond P, Weiss S, Stintzi A, Schaller A, Porzel A, García-Mina JM, Solano R (2018) An OPR3-independent pathway uses 4,5-didehydrojasmonate for jasmonate synthesis. Nat Chem Biol 14:171–178

    Article  CAS  PubMed  Google Scholar 

  • Christensen SA, Nemchenko A, Park YS, Borrego E, Huang PC, Schmelz EA, Kunze S, Feussner I, Yalpani N, Meeley R, Kolomiets MV (2014) The novel monocot-specific 9-lipoxygenase ZmLOX12 is required to mount an effective jasmonate-mediated defense against Fusarium verticillioides in maize. Mol Plant Microbe Interact 27:1263–1276

    Article  PubMed  Google Scholar 

  • Denby KJ, Kumar P, Kliebenstein DJ (2004) Identification of Botrytis cinerea susceptibility loci in Arabidopsis thaliana. Plant J 38:473–486

    Article  CAS  PubMed  Google Scholar 

  • Ellis C, Turner JG (2002) A conditionally fertile COI1 allele indicates cross-talk between plant hormone signalling pathways in Arabidopsis thaliana seeds and young seedlings. Planta 215:549–556

    Article  CAS  PubMed  Google Scholar 

  • Ferrari S, Plotnikova JM, De Lorenzo G, Ausubel FM (2003) Arabidopsis local resistance to Botrytis cinerea involves salicylic acid and camalexin and requires EDS4 and PAD2, but not SID2, EDS5 or PAD4. Plant J 35:193–205

    Article  CAS  PubMed  Google Scholar 

  • Fones HN, Fisher MC, Gurr SJ (2017) Emerging fungal threats to plants and animals challenge agriculture and ecosystem resilience. Microbiol Spectr. https://doi.org/10.1128/microbiolspec.FUNK-0027-2016

    Article  PubMed  Google Scholar 

  • Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227

    Article  CAS  PubMed  Google Scholar 

  • Gregory PJ, Johnson SN, Newton AC, Ingram JSI (2009) Integrating pests and pathogens into the climate change/food security debate. J Exp Bot 60:2827–2838

    Article  CAS  PubMed  Google Scholar 

  • Hua L, Yong C, Zhanquan Z, Boqiang L, Guozheng Q, Shiping T (2018) Pathogenic mechanisms and control strategies of Botrytis cinerea causing post-harvest decay in fruits and vegetables. Food Qual Saf 2:111–119

    Article  CAS  Google Scholar 

  • Katsir L, Schilmiller AL, Staswick PE, He SY, Howe GA (2008) COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine. Proc Natl Acad Sci USA 105:7100–7105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kliebenstein DJ, Rowe HC, Denby KJ (2005) Secondary metabolites influence Arabidopsis/Botrytis interactions: variation in host production and pathogen sensitivity. Plant J 44:25–36

    Article  CAS  PubMed  Google Scholar 

  • Koga H, Zeyen RJ, Bushnell WR, Ahlstrand GG (1988) Hypersensitive cell death, autofluorescence, and insoluble silicon accumulation in barley leaf epidermal cells under attack by Erysiphe graminis f. sp. hordei. Physiol Mol Plant Path 32:395–409

    Article  Google Scholar 

  • Laluk K, Mengiste T (2010) Necrotroph attacks on plants: wanton destruction or covert extortion? Arabidopsis Book 8:e0136

    Article  PubMed  PubMed Central  Google Scholar 

  • McKim SM, Stenvik G-E, Butenko MA, Kristiansen W, Cho SK, Hepworth SR, Aalen RB, Haughn GW (2008) The BLADE-ON-PETIOLE genes are essential for abscission zone formation in Arabidopsis. Development 135:1537–1546

    Article  CAS  PubMed  Google Scholar 

  • Mengiste T (2012) Plant immunity to necrotrophs. Annu Rev Phytopathol 50:267–294

    Article  CAS  PubMed  Google Scholar 

  • Park JH, Halitschke R, Kim HB, Baldwin IT, Feldmann KA, Feyereisen R (2002) A knock-out mutation in allene oxide synthase results in male sterility and defective wound signal transduction in Arabidopsis due to a block in jasmonic acid biosynthesis. Plant J 31:1–12

    Article  PubMed  Google Scholar 

  • Penninckx IA, Eggermont K, Terras FR, Thomma BP, De Samblanx GW, Buchala A, Métraux JP, Manners JM, Broekaert WF (1996) Pathogen-induced systemic activation of a plant defensin gene in Arabidopsis follows a salicylic acid-independent pathway. Plant Cell 8:2309–2323

    CAS  PubMed  PubMed Central  Google Scholar 

  • Raacke IC, Mueller MJ, Berger S (2006) Defects in allene oxide synthase and 12-oxa-phytodienoic acid reductase alter the resistance to Pseudomonas syringae and Botrytis cinerea. J Phytopathol 154:740–744

    Article  CAS  Google Scholar 

  • Roberts JA, Elliott KA, Gonzalez-Carranza ZH (2002) Abscission, dehiscence, and other cell separation processes. Annu Rev Plant Biol 53:131–158

    Article  CAS  PubMed  Google Scholar 

  • Rowe HC, Walley JW, Corwin J, Chan EK-F, Dehesh K, Kliebenstein DJ (2010) Deficiencies in jasmonate-mediated plant defense reveal quantitative variation in Botrytis cinerea pathogenesis. PLOS Path 6:e1000861

    Article  Google Scholar 

  • Shlezinger N, Minz A, Gur Y, Hatam I, Dagdas YF, Talbot NJ, Sharon A (2011) Anti-apoptotic machinery protects the necrotrophic fungus Botrytis cinerea from host-induced apoptotic-like cell death during plant infection. PLOS Path 7:e1002185

    Article  CAS  Google Scholar 

  • Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, He SY, Howe GA, Browse J (2007) JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling. Nature 448:661–665

    Article  CAS  PubMed  Google Scholar 

  • Thomma BPHJ, Eggermont K, Penninckx IAMA, Mauch-Mani B, Vogelsang R, Cammue BPA, Broekaert WF (1998) Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc Natl Acad Sci USA 95:15107–15111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thomma BPHJ, Nelissen I, Eggermont K, Broekaert WF (1999) Deficiency in phytoalexin production causes enhanced susceptibility of Arabidopsis thaliana to the fungus Alternaria brassicicola. Plant J 19:163–171

    Article  CAS  PubMed  Google Scholar 

  • Thomma BPHJ, Eggermont K, Broekaert WF, Cammue BPA (2000) Disease development of several fungi on Arabidopsis can be reduced by treatment with methyl jasmonate. Plant Physiol Biochem 38:421–427

    Article  CAS  Google Scholar 

  • Tronsmo A, Raa J (1977) Life cycle of the dry eye rot pathogen Botrytis cinerea Pers. on apple. Phytopathol Zeitschr 89:203–207

    Article  Google Scholar 

  • Van Kan JAL (2006) Licensed to kill: the lifestyle of a necrotrophic plant pathogen. Trends Plant Sci 11:247–253

    Article  PubMed  Google Scholar 

  • Veloso J, Van Kan JAL (2018) Many shades of grey in Botrytis-host plant interactions. Trends Plant Sci 23:613–622

    Article  CAS  PubMed  Google Scholar 

  • Veronese P, Chen X, Bluhm B, Salmeron J, Dietrich R, Mengiste T (2004) The BOS loci of Arabidopsis are required for resistance to Botrytis cinerea infection. Plant J 40:558–574

    Article  CAS  PubMed  Google Scholar 

  • Veronese P, Nakagami H, Bluhm B, AbuQamar S, Chen X, Salmeron J, Dietrich RA, Hirt H, Mengiste T (2006) The membrane-anchored BOTRYTIS-INDUCED KINASE1 plays distinct roles in Arabidopsis resistance to necrotrophic and biotrophic pathogens. Plant Cell 18:257–273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Williamson B, Tudzynski B, Tudzynski P, Van Kan JAL (2007) Botrytis cinerea: the cause of grey mould disease. Mol Plant Pathol 8:561–580

    Article  CAS  PubMed  Google Scholar 

  • Yang W, Devaiah SP, Pan X, Isaac G, Welti R, Wang X (2007) AtPLAI is an acyl hydrolase involved in basal jasmonic acid production and Arabidopsis resistance to Botrytis cinerea. J Biol Chem 282:18116–18128

    Article  CAS  PubMed  Google Scholar 

  • Zhu Z (2014) Molecular basis for jasmonate and ethylene signal interactions in Arabidopsis. J Exp Bot 65:5743–5748

    Article  CAS  PubMed  Google Scholar 

  • Zhu Z, Lee B (2015) Friends or foes: new insights in jasmonate and ethylene co-actions. Plant Cell Physiol 56:414–420

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by Rice University, China Scholarship Council (No. 201406350018 to YD), and the E&M Foundation to W-TM. Part of the research was performed using the Environmental Molecular Sciences Laboratory (EMSL), a national scientific user facility sponsored by the Department of Energy’s Office of Biological and Environmental Research and located at Pacific Northwest National Laboratory.

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Author notes

  1. Eli J. Borrego

    Present address: Thomas H. Gosnell School of Life Sciences, Rochester Institute of Technology, Rochester, NY, 14623, USA

Authors and Affiliations

  1. BioSciences Department, Rice University, Houston, TX, 77005, USA

    Yanwan Dai, Yuan Liu, Michael Huang, E. Wassim Chehab & Janet Braam

  2. Computer Science Department, Rice University, Houston, TX, 77005, USA

    Huw A. Ogilvie

  3. Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, WA, 99352, USA

    Lye Meng Markillie, Hugh D. Mitchell, Matthew J. Gaffrey & Galya Orr

  4. Department of Plant Pathology and Microbiology, Texas A&M University, College Station, TX, 77843, USA

    Eli J. Borrego & Michael V. Kolomiets

  5. Graduate Institute of Biotechnology, National Chung Hsing University, Taichung, 40227, Taiwan

    Wan-Ting Mao

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  1. Yanwan Dai
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Correspondence to Janet Braam.

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Dai, Y., Ogilvie, H.A., Liu, Y. et al. Rosette core fungal resistance in Arabidopsis thaliana. Planta 250, 1941–1953 (2019). https://doi.org/10.1007/s00425-019-03273-5

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