Skip to main content

Advertisement

SpringerLink
Log in

Histological and molecular studies of the non-host interaction between wheat and Uromyces fabae

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Non-host resistance (NHR) confers plant species immunity against the majority of microbes. As an important crop, wheat can be damaged by several Puccinia species but is immune to all Uromyces species. Here, we studied the basis of NHR in wheat against the broad bean rust pathogen Uromyces fabae (Uf). In the wheat–Uf interaction, microscopic observations showed that urediospores germinated efficiently on wheat leaves. However, over 98% of the germ tubes failed to form appressoria over stomata. For the few that invaded through stomata, the majority of them failed to penetrate wheat mesophyll cells. At 96 hours after inoculation, less than 4% of the Uf infection units that had entered the mesophyll tissue formed haustoria. Attempted penetration by haustorium mother cells induced the thickening of cell wall and the formation of papillae in plant cells, which arrested the development or growth of Uf penetration pegs. For the Uf haustoria formed in wheat cells, they were encased in callose-like materials and did not elicit hypersensitive response. Localized accumulation of H2O2 were observed in plant cell walls, papillae and encasement of haustoria during the wheat–Uf interaction. Furthermore, quantitative RT-PCR analysis showed that several genes involved in basal resistance and oxidative stress responses were up-regulated during Uf infection. In conclusion, our study revealed the cytological and molecular bases of NHR in wheat against the non-adapted rust fungus Uf, and highlighted the significance of papilla production in the prehaustorial NHR.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

CWA:

Cell wall apposition

DAB :

3,3-diaminobenzidine

DIC:

Differential interference contrast

dai:

Days after inoculation

hai:

Hours after inoculation

HMC:

Haustorial mother cell

HR:

Hypersensitive response

MAMPS or PAMPs:

Microbial- or pathogen-associated molecular patterns

MVBs:

Multivesicular bodies

NBT:

Nitroblue tetrazolium

NHR:

Non-host resistance

Pgt :

P. graminis f. sp. tritici

PRRs:

Pattern recognition receptors

Pst :

P. striiformis f. sp. tritici

Pt :

P. triticina

PTI:

PAMP-triggered immunity

qRT-PCR:

Quantitative RT-PCR

ROS:

Reactive oxygen species

SA:

Salicylic acid

TaAPX :

Ascorbate-peroxidase

TaCAT :

Catalase

TaPAL :

Phenylalanine ammonia lyase

TaPR1 :

Pathogenesis-related protein 1

TaPR2 :

β-1,3-glucanase

TaPR3 :

Chitinase

TaPR5 :

Thaumatin-like

TaSOD :

Superoxide dismutase

TEM:

Transmission electron microscope

Uf :

Uromyces fabae

References

  • Adhikari TB, Bai JF, Meinhardt SW, Gurung S, Myrfield M, Patel J et al (2009) Tsn1-mediated host responses to ToxA from Pyrenophora tritici-repentis. Mol Plant Microbe Interact 22:1056–1068

    Article  PubMed  CAS  Google Scholar 

  • Allen EA, Hazen BE, Hoch HC, Kwon Y, Leinhos GME, Staples RC et al (1991) Appressorium formation in response to topographical signals by 27 rust species. Phytopathology 81:323–331

    Article  Google Scholar 

  • Bhuiyan N, Selvaraj G, Wei YD, King J (2009) Gene expression profiling and silencing reveal that monolignol biosynthesis plays a critical role in penetration defence in wheat against powdery mildew invasion. J Exp Bot 60:509–521

    Article  PubMed  CAS  Google Scholar 

  • Collins NC, Thordal-Christensen H, Lipka V, Bau S, Kombrink E, Qiu JL et al (2003) SNARE-protein-mediated disease resistance at the plant cell wall. Nature 425:973–977

    Article  PubMed  CAS  Google Scholar 

  • Coram TE, Wang MN, Chen XM (2008) Transcriptome analysis of the wheat–Puccinia striiformis f. sp tritici interaction. Mol Plant Pathol 9:157–169

    Article  PubMed  CAS  Google Scholar 

  • Croxdale JL (2000) Stomatal patterning in angiosperms. Am J Bot 87:1069–1080

    Article  PubMed  CAS  Google Scholar 

  • Deising HB, Werner S, Wernitz M (2000) The role of fungal appressoriain plant infection. Microbes Infect 2:1631–1641

    Article  PubMed  CAS  Google Scholar 

  • Freialdenhoven A, Peterhansel C, Kurth J, Kreuzaler F, Schulze-Lefert P (1996) Identification of genes required for the function of non-race-specific mlo resistance to powdery mildew in barley. Plant Cell 8:5–14

    Article  PubMed  CAS  Google Scholar 

  • Hardham AR (2007) Cell biology of fungal and Oomycete infection of plants. In: Howard RJ, Gow NAR (eds) The Mycota VIII. Biology of the fungal cell, 2nd edn. Springer, Berlin, pp 251–290

    Chapter  Google Scholar 

  • Heath MC (1974) Light and electron microscope studies of the interactions of host and non-host plants with cowpea rust—Uromyces phaseoli var. vignae. Physiol Plant Pathol 4:403–408

    Article  Google Scholar 

  • Heath MC (1979) Partial characterization of the electron-opaque deposits formed in the non-host plant, French bean after cowpea rust infection. Physiol Plant Pathol 15:141–144

    Article  Google Scholar 

  • Heath MC (1981) Resistance of plants to rust infection. Phytopathology 71:971–974

    Article  Google Scholar 

  • Heath MC (2000) Nonhost resistance and nonspecific plant defences. Curr Opin Plant Biol 3:315–319

    Article  PubMed  CAS  Google Scholar 

  • Hoogkamp TJH, Chen WQ, Niks RE (1998) Specificity of prehaustorial resistance to Puccinia hordei and to two inappropriate rust fungi in barley. Phytopathology 88:856–861

    Article  PubMed  CAS  Google Scholar 

  • Huckelhoven R, Dechert C, Kogel KH (2001) Non-host resistance of barley is associated with a hydrogen peroxide burst at sites of attempted penetration by wheat powdery mildew fungus. Mol Plant Pathol 2:199–205

    Article  PubMed  CAS  Google Scholar 

  • Hulber SH, Bai J, Fellers JP, Pacheco MG, Bowden RL (2007) Gene expression patterns in near isogenic lines for wheat rust resistance gene Lr34/Yr18. Phytopathology 97:1083–1093

    Article  Google Scholar 

  • Jafary H, Albertazzi G, Marcel TC, Niks RE (2008) High diversity of genes for nonhost resistance of barley to heterologous rust fungi. Genetics 178:2327–2339

    Article  PubMed  CAS  Google Scholar 

  • Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329

    Article  PubMed  CAS  Google Scholar 

  • Kang Z, Huang L, Buchenauer H (2002) Ultrastructural changes and localization of lignin and callose in compatible and incompatible interactions between wheat and Puccinia striiformis. J Plant Dis Prot 109:25–37

    CAS  Google Scholar 

  • Kang ZS, Wan GY, Huang LL, Wei GR, Zhao J (2003) Histology and ultrastructure of incompatible combination between Puccinia striiformis and wheat cultivars with low reaction type resistance. Agric Sci China 2:1102–1113

    Google Scholar 

  • Kolmer JA, Ordonez ME, Groth JV (2009) The rust fungi. In: Encyclopedia of life sciences (ELS). Wiley, Chichester. doi:10.1002/9780470015902.a0021264

    Google Scholar 

  • Laisk A, Oja V, Kull K (1980) Statistical distribution of stomatal apertures of Vicia faba and Hordeum vulgare and the Spannungsphase of stomatal opening. J Exp Bot 31:49–58

    Article  Google Scholar 

  • Lin KC, Bushnell WR, Szabo LJ, Smith AG (1996) Isolation and expression of a host response gene family encoding thaumatin-like proteins in incompatible oat-stem rust fungus interactions. Mol Plant Microbe Interact 9:511–522

    Article  PubMed  CAS  Google Scholar 

  • Lipka V, Dittgen J, Bednarek P, Bhat R, Wiermer M, Stein M et al (2005) Pre- and postinvasion defences both contribute to nonhost resistance in Arabidopsis. Science 310:1180–1183

    Article  PubMed  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402–408

    Article  PubMed  CAS  Google Scholar 

  • Loehrer M, Langenbach C, Goellner K, Conrath U, Schaffrath U (2008) Characterization of nonhost resistance of Arabidopsis to the Asian soybean rust. Mol Plant Microbe Interact 21:1421–1430

    Article  PubMed  CAS  Google Scholar 

  • Mauch F, Mauch-Mani B, Boller T (1988) Antifungal hydrolases in pea tissue. II. Inhibition of fungal growth by combinations of chitinase and β-1, 3-glucanase. Plant Physiol 88:936–942

    Article  PubMed  CAS  Google Scholar 

  • Mellersh DG, Heath MC (2003) An investigation into the involvement of defense signaling pathways in components of the nonhost resistance of Arabidopsis thaliana to rust fungi also reveals a model system for studying rust fungal compatibility. Mol Plant Microbe Interact 16:398–404

    Article  PubMed  CAS  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  PubMed  CAS  Google Scholar 

  • Mysore KS, Ryu CM (2004) Nonhost resistance: how much do we know? Trends Plant Sci 9:97–104

    Article  PubMed  CAS  Google Scholar 

  • Niks RE (1983a) Comparative histology of partial resistance and the nonhost reaction to leaf rust pathogens in barley and wheat seedlings. Phytopathology 73:60–64

    Article  Google Scholar 

  • Niks RE (1983b) Haustorium formation by Puccinia hordei in leaves of hypersensitive, partially resistant, and nonhost plant genotypes. Phytopathology 73:64–66

    Article  Google Scholar 

  • Niks RE, Marcel TC (2009) Non-host and basal resistance: how to explain specificity? New Phytol 182:817–828

    Article  PubMed  Google Scholar 

  • Orczyk W, Dmochowska-Boguta M, Czembor HJ, Nadolska-Orczyk A (2010) Spatiotemporal patterns of oxidative burst and micronecrosis in resistance of wheat to brown rust infection. Plant Pathol 59:567–575

    Article  Google Scholar 

  • Pritsch C, Muehlbauer GJ, Bushnell WR, Somers DA, Vance CP (2000) Fungal development and induction of defense response genes during early infection of wheat spikes by Fusarium graminearum. Mol Plant Microbe Interact 13:159–169

    Article  PubMed  CAS  Google Scholar 

  • Rodrigues P, Garrood JM, Shen QH, Smith PH, Boyd LA (2004) The genetics of non-host disease resistance in wheat to barley yellow rust. Theor Appl Genet 109:425–432

    Article  PubMed  CAS  Google Scholar 

  • Schaffrath U, Freydl E, Dudler R (1997) Evidence for different signaling pathways activated by inducers of acquired resistance in wheat. Mol Plant Microbe Interact 10:779–783

    Article  CAS  Google Scholar 

  • Schweizer P (2007) Nonhost resistance of plants to powdery mildew—new opportunities to unravel the mystery. Physiol Mol Plant Pathol 70:3–7

    Article  CAS  Google Scholar 

  • Shafiei R, Hang C, Kang JG, Loake GJ (2007) Identification of loci controlling non-host disease resistance in Arabidopsis against the leaf rust pathogen Puccinia triticina. Mol Plant Pathol 8:773–784

    Article  PubMed  CAS  Google Scholar 

  • Sillero JC, Rubiales D (2002) Histological characterization of resistance to Uromyces viciae-fabae in faba bean. Phytopathology 92:294–299

    Article  PubMed  CAS  Google Scholar 

  • Southerton SG, Deverall BJ (1990) Histochemical and chemical evidence for lignin accumulation during the expression of resistance to leaf rust fungi in wheat. Physiol Mol Plant Pathol 36:483–494

    Article  CAS  Google Scholar 

  • Stein M, Dittgen J, Sanchez-Rodriguez C, Hou BH, Molina A, Schulze-Lefert P et al (2006) Arabidopsis PEN3/PDR8, an ATP cassette transporter, contributes to nonhost resistance to inappropriate pathogens that enter by direct penetration. Plant Cell 18:731–746

    Article  PubMed  CAS  Google Scholar 

  • Thordal-Christensen H (2003) Fresh insight into processes of nonhost resistance. Curr Opin Plant Biol 6:351–357

    Article  PubMed  CAS  Google Scholar 

  • Thordal-Christensen H, Zhang Z, Wei YD, Collinge DB (1997) Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley–powdery mildew interaction. Plant J 11:1187–1194

    Article  CAS  Google Scholar 

  • Tufan HA, McGrann GRD, Magusin A, Morel JB, Miché L, Boyd LA (2009) Wheat Blast: histopathology and transcriptome reprogramming in response to adapted and non-adapted Magnaporthe isolates. New Phytol 184:473–484

    Article  PubMed  Google Scholar 

  • Van Loon LC, Van Strien EA (1999) The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiol Mol Plant Pathol 55:85–97

    Article  Google Scholar 

  • Voegele RT (2006) Uromyces fabae: development, metabolism, and interactions with its host Vicia faba. FEMS Microbiol Lett 259:165–173

    Article  PubMed  CAS  Google Scholar 

  • Wang CF, Huang LL, Buchenauer H, Han QM, Zhang HC, Kang ZS (2007) Histochemical studies of the accumulation of reactive oxygen species(O2 − and H2O2) in the incompatible and compatible interaction of wheat–Puccinia striiformis f.sp. tritici. Physiol Mol Plant Pathol 71:230–239

    Article  CAS  Google Scholar 

  • Wang XJ, Tang CL, Zhang G, Li YC, Wang CF, Liu B et al (2009) cDNA-AFLP analysis reveals differential gene expression in compatible interaction of wheat challenged with Puccinia striiformis f. sp. tritici. BMC Genomics 10:289

    Article  PubMed  CAS  Google Scholar 

  • Whetten R, Sederoff R (1995) Lignin biosynthesis. Plant Cell 7:1001–1013

    Article  PubMed  CAS  Google Scholar 

  • Yu XM, Wang XJ, Wang CF, Chen XM, Qu ZP, Yu XD et al (2010) Wheat defense genes in fungal (Puccinia striiformis) infection. Funct Integr Genomics 10:227–239

    Article  PubMed  CAS  Google Scholar 

  • Zipfel C (2008) Pattern-recognition receptors in plant innate immunity. Curr Opin Immunol 20:10–16

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by grants from National Basic Research Program of China (No. 2006CB100203), Modern Agro-industry Technology Research System in China, the National Natural Science Foundation of China (No. 30930064), and the 111 Project from the Ministry of Education of China (B07049).

Author information

Authors and Affiliations

  1. State Key Laboratory of Crop Stress Biology for Arid Areas and College of Plant Protection, Northwest A&F University Yangling, Shaanxi, 712100, People’s Republic of China

    Hongchang Zhang, Chenfang Wang, Yulin Cheng, Xiaojie Wang, Feng Li, Qingmei Han, Jinrong Xu, Lili Huang, Guorong Wei & Zhensheng Kang

  2. College of Life Sciences, Northwest A&F University, Yangling, Shaanxi, 712100, People’s Republic of China

    Hongchang Zhang

  3. Department of Botany and Plant Pathology, Purdue University, West Lafayette, IN, 47907, USA

    Jinrong Xu

  4. USDA-ARS and Department of Plant Pathology, Washington State University, Pullman, WA, 99164-6430, USA

    Xianming Chen

Authors
  1. Hongchang Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chenfang Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yulin Cheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xiaojie Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Feng Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Qingmei Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jinrong Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Xianming Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Lili Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Guorong Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Zhensheng Kang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhensheng Kang.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhang, H., Wang, C., Cheng, Y. et al. Histological and molecular studies of the non-host interaction between wheat and Uromyces fabae . Planta 234, 979–991 (2011). https://doi.org/10.1007/s00425-011-1453-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-011-1453-5

Keywords

Search

Navigation