Skip to main content

Haustorium Initiation and Early Development

  • Chapter
  • First Online:
Parasitic Orobanchaceae

Abstract

The haustoria of the Orobanchaceae are formed in response to chemical and physical stimuli provided by host roots. Several quinones and phenols have been identified that induce haustorium development, suggesting that parasites recognise a multiplicity of molecules in the rhizosphere associated with host roots. In some cases the parasite activates host cell wall peroxidases which generate haustorium-inducing factors. The redox states of the molecules are critical for activity. Transitions from oxidised quinones to reduced phenols generate semiquinone intermediates that initiate haustorium differentiation. Signalling is interrupted by inhibiting quinone oxidoreductases in the parasite through gene silencing. This chapter reviews our current state of knowledge about early haustorium development in Orobanchaceae with particular emphasis on how haustorium-inducing molecules are recognised by parasitic plants.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Ahmad P, Sarwat M, Sharma S (2008) Reactive oxygen species, antioxidants and signaling in plants. J Plant Biol 51:167–173

    Article  CAS  Google Scholar 

  • Albrecht H, Yoder JI, Phillips DA (1999) Flavonoids promote haustoria formation in the root parasite Triphysaria. Plant Physiol 119:585–591

    Article  PubMed  CAS  Google Scholar 

  • Appel HM (1993) Phenolics in ecological interactions – the importance of oxidation. J Chem Ecol 19:1521–1552

    Article  CAS  Google Scholar 

  • Atsatt PR (1973) Parasitic flowering plants: how did they evolve? Am Nat 107:502–510

    Article  Google Scholar 

  • Atsatt P, Strong D (1970) The population biology of annual grassland hemiparasites: I. The host environment. Evolution 24:278–291

    Article  Google Scholar 

  • Atsatt PR, Hearn TF, Nelson RL, Heineman RT (1978) Chemical induction and repression of haustoria in Orthocarpus purpurascens (Scophulariaceae). Ann Bot 42:1177–1184

    CAS  Google Scholar 

  • Attawi FAJ, Weber HC (1980) Zum Parasitismus und zum morphologisch-anatomischen Struktur der Sekundärhaustorien von Orobanche-Arten (Orobanchaceae). Flora 169:55–83

    Google Scholar 

  • Baird WV, Riopel JL (1984) Experimental studies of haustorium initiation and early development in Agalinis purpurea (L.) Raf. (Scrophulariaceae). Am J Bot 71:803–814

    Article  Google Scholar 

  • Baird WV, Riopel JL (1985) Surface characteristics of root haustorial hairs of parasitic Scrophulariaceae. Bot Gaz 146:63–69

    Article  Google Scholar 

  • Bandaranayake PCG, Filappova T, Tomilov A, Tomilova NB, Jamison-McClung D, Ngo Q, Inoue K, Yoder JI (2010) A single-electron reducing quinone oxidoreductase is necessary to induce haustorium development in the root parasitic plant Triphysaria. Plant Cell 22:1404–1419

    Article  PubMed  CAS  Google Scholar 

  • Bandaranayake PC, Tomilov A, Tomilova NB, Ngo QA, Wickett N, dePamphilis CW, Yoder JI (2012) The TvPirin gene is necessary for haustorium development in the parasitic plant Triphysaria versicolor. Plant Physiol 158:1046–1053

    Article  PubMed  CAS  Google Scholar 

  • Caldwell ES, Steelink C (1969) Phenoxy radical intermediate in the enzymatic degradation of lignin model compounds. Biochim Biophys Acta 184:420–431

    Article  PubMed  CAS  Google Scholar 

  • Carol RJ, Dolan L (2006) The role of reactive oxygen species in cell growth: lessons from root hairs. J Exp Bot 57:1829–1834

    Article  PubMed  CAS  Google Scholar 

  • Chang M, Lynn DG (1986) The haustorium and the chemistry of host recognition in parasitic angiosperms. J Chem Ecol 12:561–579

    Article  CAS  Google Scholar 

  • Conn EE (ed) (1986) Recent advances in phytochemistry: the shikimic acid pathway, vol 20. Plenum, New York

    Google Scholar 

  • Davis CC, Wurdack KJ (2004) Host-to-parasite gene transfer in flowering plants: phylogenetic evidence from Malpighiales. Science 305:676–678

    Article  PubMed  CAS  Google Scholar 

  • Estabrook EM, Yoder JI (1998) Plant-plant communications: rhizosphere signalling between parasitic angiosperms and their hosts. Plant Physiol 116:1–7

    Article  CAS  Google Scholar 

  • Flagel LE, Wendel JF (2009) Gene duplication and evolutionary novelty in plants. New Phytol 183:557–564

    Article  PubMed  Google Scholar 

  • Floyd SK, Bowman JL (2007) The ancestral developmental tool kit of land plants. Int J Plant Sci 168:1–35

    Article  CAS  Google Scholar 

  • Foreman J, Demidchik V, Bothwell JH, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JD, Davies JM, Dolan L (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–446

    Article  PubMed  CAS  Google Scholar 

  • Foyer CH, Noctor G (2009) Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid Redox Signal 11:861–905

    Article  PubMed  CAS  Google Scholar 

  • Geurts R, Fedorova E, Bisseling T (2005) Nod factor signaling genes and their function in the early stages of Rhizobium infection. Curr Opin Plant Biol 8:346–352

    Article  PubMed  CAS  Google Scholar 

  • Gibson CC, Watkinson AR (1989) The host range and selectivity of a parasitic plant: Rhinanthus minor L. Oecologia 78:401–406

    Article  Google Scholar 

  • Goldwasser Y, Westwood JH, Yoder JI (2002) The use of Arabidopsis to study interactions between parasitic angiosperms and their plant hosts. In: Somerville C, Meyerowitz E (eds) The Arabidopsis book. American Society Plant Biologists, Rockville, MD, pp 1–17

    Google Scholar 

  • Hegarty MJ, Hiscock SJ (2008) Genomic clues to the evolutionary success of polyploid plants. Curr Biol 18:R435–R444

    Article  PubMed  CAS  Google Scholar 

  • Heide-Jørgensen HS (2008) Parasitic flowering plants. Brill Academic, Leiden, NL

    Book  Google Scholar 

  • Hood ME, Condon JM, Timko MP, Riopel JL (1998) Primary haustorial development of Striga asiatica on host and nonhost species. Phytopathology 88:70–75

    Article  PubMed  CAS  Google Scholar 

  • Jamison DS, Yoder JI (2001) Heritable variation in quinone-induced haustorium development in the parasitic plant Triphysaria. Plant Physiol 125:1870–1879

    Article  PubMed  CAS  Google Scholar 

  • Joel DM, Losner-Goshen D (1994) The attachment organ of the parasitic angiosperms Orobanche cumana and O. aegyptiaca and its development. Can J Bot 72:564–574

    Article  Google Scholar 

  • Keyes WJ, O’Malley RC, Kim D, Lynn DG (2000) Signaling organogenesis in parasitic angiosperms: xenognosin generation, perception, and response. J Plant Growth Regul 19:217–231

    PubMed  CAS  Google Scholar 

  • Keyes WJ, Taylor JV, Apkarian RP, Lynn DG (2001) Dancing together. Social controls in parasitic plant development. Plant Physiol 127:1508–1512

    Article  PubMed  CAS  Google Scholar 

  • Keyes WJ, Palmer AG, Erbil WK, Taylor JV, Apkarian RP, Weeks ER, Lynn DG (2007) Semagenesis and the parasitic angiosperm Striga asiaticae. Plant J 51:707–716

    Article  PubMed  CAS  Google Scholar 

  • Krisnangkura K, Gold MH (1979) Peroxidase catalysed oxidative decarboxylation of vanillic acid to methoxy-p-hydroquinone. Phytochemistry 18:2019–2021

    Article  CAS  Google Scholar 

  • Kuijt J (1969) The biology of parasitic flowering plants. University of California Press, Berkeley, CA

    Google Scholar 

  • Li JX, Timko MP (2009) Gene-for-gene resistance in Striga-Cowpea associations. Science 325:1094

    Article  PubMed  CAS  Google Scholar 

  • Liszkay A, van der Zalm E, Schopfer P (2004) Production of reactive oxygen intermediates O2 ˙−, H2O2, and Ë™OH, by maize roots and their role in wall loosening and elongation growth. Plant Physiol 136:3114–3123

    Article  PubMed  CAS  Google Scholar 

  • Lynn DG, Chang M (1990) Phenolic signals in cohabitation: implications for plant development. Ann Rev Plant Physiol Plant Mol Biol 41:497–526

    Article  CAS  Google Scholar 

  • Lynn DG, Steffens JC, Kamat VS, Graden DW, Shabanowitz J, Riopel JL (1981) Isolation and characterization of the first host recognition substance for parasitic angiosperms. J Am Chem Soc 103:1868–1870

    Article  CAS  Google Scholar 

  • Mano J, Babiychuk E, Belles-Boix E, Hiratake J, Kimura A, Inzea D, Kushnir S, Asada K (2000) A novel NADPH : diamide oxidoreductase activity in Arabidopsis thaliana P1 zeta-crystallin. Eur J Biochem 267:3661–3671

    Article  PubMed  CAS  Google Scholar 

  • Matvienko M, Torres MJ, Yoder JI (2001a) Transcriptional responses in the hemiparasitic plant Triphysaria versicolor to host plant signals. Plant Physiol 127:272–282

    Article  PubMed  CAS  Google Scholar 

  • Matvienko M, Wojtowicz A, Wrobel R, Jamison D, Goldwasser Y, Yoder JI (2001b) Quinone oxidoreductase message levels are differentially regulated in parasitic and non-parasitic plants exposed to allelopathic quinones. Plant J 25:375–387

    Article  PubMed  CAS  Google Scholar 

  • Mitra RM, Gleason CA, Edwards A, Hadfield J, Downie JA, Oldroyd GED, Long SR (2004) A Ca 2+ /calmodulin-dependent protein kinase required for symbiotic nodule development: gene identification by transcript-based cloning. Proc Natl Acad Sci USA 101:4701–4705

    Article  PubMed  CAS  Google Scholar 

  • Mou Z, Fan WH, Dong XN (2003) Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113:935–944

    Article  PubMed  CAS  Google Scholar 

  • Mower JP, Stefanovic S, Young GJ, Palmer JD (2004) Plant genetics: gene transfer from parasitic to host plants. Nature 432:165–166

    Article  PubMed  CAS  Google Scholar 

  • Musselman LJ, Dickison WC (1975) The structure and development of the haustorium in parasitic Scrophulariaceae. Bot J Linn Soc 70:183–212

    Article  Google Scholar 

  • Nester EW, Gordon MP, Kerr A (2005) Agrobacterium tumefaciens: from plant pathology to biotechnology. APS Press, St. Paul, MN

    Google Scholar 

  • Nickrent DL, Musselman LJ, Riopel JL, Eplee RE (1979) Haustorial initiation and non-host penetration in witchweed (Striga asiatica). Ann Bot 43:233–236

    Google Scholar 

  • Nwoke F, Okonkwo SNC (1978) Structure and development of the primary haustorium in Alectra vogelii Benth. Ann Bot 42:447–454

    Google Scholar 

  • O’Brien P (1991) Molecular mechanisms of quinone toxicity. Chem Biol Interact 80:1–41

    Article  PubMed  Google Scholar 

  • O’Malley RC, Lynn DG (2000) Expansin message regulation in parasitic angiosperms: marking time in development. Plant Cell 12:1455–1465

    PubMed  Google Scholar 

  • Okonkwo SNC (1966) Studies of Striga senegalensis Benth. I. Mode of host-parasite union and haustorial structure. Phytomorphology 16:453–463

    Google Scholar 

  • Okonkwo SNC, Nwoke FIO (1978) Initiation, development and structure of the primary haustorium in Striga gesnerioides (Scrophulariaceae). Ann Bot 42:455–463

    Google Scholar 

  • Olivier A, Benhamou N, Leroux GD (1991) Cell surface interactions between sorghum roots and the parasitic weed Striga hermonthica: cytochemical aspects of cellulose distribution in resistant and susceptible host tissues. Can J Bot 69:1679–1690

    Article  Google Scholar 

  • Palmer AG, Chen MC, Kinger NP, Lynn DG (2009) Parasitic angiosperms, semagenesis and general strategies for plant-plant signaling in the rhizosphere. Pest Manag Sci 65:512–519

    Article  PubMed  CAS  Google Scholar 

  • Rao PV, Krishna CM, Zigler JS (1992) Identification and characterization of the enzymatic activity of zeta-crystallin from guinea pig lens – a novel NADPH-quinone oxidoreductase. J Biol Chem 267:96–102

    PubMed  CAS  Google Scholar 

  • Rich PJ, Grenier C, Ejeta G (2004) Striga resistance in the wild relatives of sorghum. Crop Sci 44:2221–2229

    Article  Google Scholar 

  • Riopel JL (1983) The biology of parasitic plants: physiological aspects. In: Moore R (ed) Vegetative compatibility. Academic, New York, pp 13–34

    Google Scholar 

  • Riopel JL, Baird WV (1987) Morphogenesis of the early development of primary haustoria in Striga asiatica. In: Musselman LJ (ed) Parasitic weeds in agriculture. CRC, Boca Raton, FL, pp 107–125

    Google Scholar 

  • Riopel J, Musselman L (1979) Experimental initiation of haustoria in Agalinis purpurea. Am J Bot 66:570–575

    Article  Google Scholar 

  • Riopel JL, Timko MP (1995) Haustorial initiation and differentiation. In: Press MC, Graves JD (eds) Parasitic plants. Chapman and Hall, London, pp 39–79

    Google Scholar 

  • Ross D, Siegel D, Helmut S, Lester P (2004) NAD(P)H:quinone oxidoreductase 1 (NQO1, DT-diaphorase), functions and pharmacogenetics. In: Sies H, Packer L (eds) Methods in enzymology. Academic, London, pp 115–144

    Google Scholar 

  • Saunders AR (1933) Studies in phanerogamic parasitism with particular reference to Striga lutea. Sci Bull Union S Afr Dep Agric 128:5–56

    Google Scholar 

  • Smith CE, Ruttledge T, Zeng Z, O’Malley RC, Lynn DG (1996) A mechanism for inducing plant development – the genesis of a specific inhibitor. Proc Natl Acad Sci USA 93:6986–6991

    Article  PubMed  CAS  Google Scholar 

  • Sparla F, Tedeschi G, Trost P (1996) NAD(P)H-(quinone-acceptor) oxidoreductase of tobacco leaves is a flavin mononucleotide-containing flavoenzyme. Plant Physiol 112:249–258

    PubMed  CAS  Google Scholar 

  • Steffens JC, Lynn DG, Kamat VS, Riopel JL (1982) Molecular specificity of haustorial induction in Agalinis purpurea (L.) Raf. (Scrophulariaceae). Ann Bot 50:1–7

    CAS  Google Scholar 

  • Testa B (1995) The metabolism of drugs and other xenobiotics: biochemistry of redox reactions. Academic, New York

    Google Scholar 

  • Tomilov AA, Tomilova NB, Abdallah I, Yoder JI (2005) Localized hormone fluxes and early haustorium development in the hemiparasitic plant Triphysaria versicolor. Plant Physiol 138:1469–1480

    Article  PubMed  CAS  Google Scholar 

  • Torres MJ, Tomilov AA, Tomilova N, Reagan RL, Yoder JI (2005) Pscroph, a parasitic plant EST database enriched for parasite associated transcripts. BMC Plant Biol 5:24

    Article  PubMed  Google Scholar 

  • Visser JH, Dörr I, Kollman D (1990) On the parasitism of Alectra vogelii Benth (Scrophulariaceae) 1. Early development of the primary haustorium and initiation of the stem. Z Pflanzenphysiol 84:213–222

    Article  Google Scholar 

  • Werth C, Riopel JL (1979) A study of the host range of Aureolaria pedicularia (L.) Raf. (Scrophulariaceae). Am Midl Nat 102:300–306

    Article  Google Scholar 

  • Westwood JH, Yoder JI, Timko MP, dePamphilis CW (2010) The evolution of parasitism in plants. Trends Plant Sci 15:227–235

    Article  PubMed  CAS  Google Scholar 

  • William CN (1961) Growth and morphogenesis of Striga seedlings. Nature 189:378–381

    Article  Google Scholar 

  • Wolf SJ, Timko MP (1991) In vitro root culture – a novel approach to study the obligate parasite Striga asiatica (L) Kuntze. Plant Sci 73:233–242

    Article  CAS  Google Scholar 

  • Wrobel RL, Yoder JI (2001) Differential RNA expression of alpha-expansin gene family members in the parasitic angiosperm Triphysaria versicolor (Scrophulariaceae). Gene 266:85–93

    Article  PubMed  CAS  Google Scholar 

  • Wrobel RL, Matvienko M, Yoder JI (2002) Heterologous expression and biochemical characterization of an NAD(P)H : quinone oxidoreductase from the hemiparasitic plant Triphysaria versicolor. Plant Physiol Biochem 40:265–272

    Article  CAS  Google Scholar 

  • Yoder JI (1997) A species-specific recognition system directs haustorium development in the parasitic plant Triphysaria (Scrophulariaceae). Planta 202:407–413

    Article  PubMed  CAS  Google Scholar 

  • Yoder JI (1999) Parasitic plant responses to host plant signals: a model for subterranean plant–plant interactions. Curr Opin Plant Biol 2:65–70

    Article  PubMed  CAS  Google Scholar 

  • Yoshida S, Maruyama S, Nozaki H, Shirasu K (2010) Horizontal gene transfer by the parasitic plant Striga hermonthica. Science 328:1128

    Article  PubMed  CAS  Google Scholar 

  • Zeng ZX, Cartwright CH, Lynn DG (1996) Cyclopropyl-p-benzoquinone – a specific organogenesis inhibitor in plants. J Am Chem Soc 118:1233–1234

    Article  CAS  Google Scholar 

  • Zhou WJ, Yoneyama K, Takeuchi Y, Iso S, Rungmekarat S, Chae SH, Sato D, Joel DM (2004) In vitro infection of host roots by differentiated calli of the parasitic plant Orobanche. J Exp Bot 55:899–907

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to John I. Yoder .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Bandaranayake, P.C.G., Yoder, J.I. (2013). Haustorium Initiation and Early Development. In: Joel, D., Gressel, J., Musselman, L. (eds) Parasitic Orobanchaceae. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-38146-1_4

Download citation

Publish with us

Policies and ethics