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.
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References
Ahmad P, Sarwat M, Sharma S (2008) Reactive oxygen species, antioxidants and signaling in plants. J Plant Biol 51:167–173
Albrecht H, Yoder JI, Phillips DA (1999) Flavonoids promote haustoria formation in the root parasite Triphysaria. Plant Physiol 119:585–591
Appel HM (1993) Phenolics in ecological interactions – the importance of oxidation. J Chem Ecol 19:1521–1552
Atsatt PR (1973) Parasitic flowering plants: how did they evolve? Am Nat 107:502–510
Atsatt P, Strong D (1970) The population biology of annual grassland hemiparasites: I. The host environment. Evolution 24:278–291
Atsatt PR, Hearn TF, Nelson RL, Heineman RT (1978) Chemical induction and repression of haustoria in Orthocarpus purpurascens (Scophulariaceae). Ann Bot 42:1177–1184
Attawi FAJ, Weber HC (1980) Zum Parasitismus und zum morphologisch-anatomischen Struktur der Sekundärhaustorien von Orobanche-Arten (Orobanchaceae). Flora 169:55–83
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
Baird WV, Riopel JL (1985) Surface characteristics of root haustorial hairs of parasitic Scrophulariaceae. Bot Gaz 146:63–69
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
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
Caldwell ES, Steelink C (1969) Phenoxy radical intermediate in the enzymatic degradation of lignin model compounds. Biochim Biophys Acta 184:420–431
Carol RJ, Dolan L (2006) The role of reactive oxygen species in cell growth: lessons from root hairs. J Exp Bot 57:1829–1834
Chang M, Lynn DG (1986) The haustorium and the chemistry of host recognition in parasitic angiosperms. J Chem Ecol 12:561–579
Conn EE (ed) (1986) Recent advances in phytochemistry: the shikimic acid pathway, vol 20. Plenum, New York
Davis CC, Wurdack KJ (2004) Host-to-parasite gene transfer in flowering plants: phylogenetic evidence from Malpighiales. Science 305:676–678
Estabrook EM, Yoder JI (1998) Plant-plant communications: rhizosphere signalling between parasitic angiosperms and their hosts. Plant Physiol 116:1–7
Flagel LE, Wendel JF (2009) Gene duplication and evolutionary novelty in plants. New Phytol 183:557–564
Floyd SK, Bowman JL (2007) The ancestral developmental tool kit of land plants. Int J Plant Sci 168:1–35
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
Foyer CH, Noctor G (2009) Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid Redox Signal 11:861–905
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
Gibson CC, Watkinson AR (1989) The host range and selectivity of a parasitic plant: Rhinanthus minor L. Oecologia 78:401–406
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
Hegarty MJ, Hiscock SJ (2008) Genomic clues to the evolutionary success of polyploid plants. Curr Biol 18:R435–R444
Heide-Jørgensen HS (2008) Parasitic flowering plants. Brill Academic, Leiden, NL
Hood ME, Condon JM, Timko MP, Riopel JL (1998) Primary haustorial development of Striga asiatica on host and nonhost species. Phytopathology 88:70–75
Jamison DS, Yoder JI (2001) Heritable variation in quinone-induced haustorium development in the parasitic plant Triphysaria. Plant Physiol 125:1870–1879
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
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
Keyes WJ, Taylor JV, Apkarian RP, Lynn DG (2001) Dancing together. Social controls in parasitic plant development. Plant Physiol 127:1508–1512
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
Krisnangkura K, Gold MH (1979) Peroxidase catalysed oxidative decarboxylation of vanillic acid to methoxy-p-hydroquinone. Phytochemistry 18:2019–2021
Kuijt J (1969) The biology of parasitic flowering plants. University of California Press, Berkeley, CA
Li JX, Timko MP (2009) Gene-for-gene resistance in Striga-Cowpea associations. Science 325:1094
Liszkay A, van der Zalm E, Schopfer P (2004) Production of reactive oxygen intermediates O2 ˙−, H2O2, and ˙OH, by maize roots and their role in wall loosening and elongation growth. Plant Physiol 136:3114–3123
Lynn DG, Chang M (1990) Phenolic signals in cohabitation: implications for plant development. Ann Rev Plant Physiol Plant Mol Biol 41:497–526
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
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
Matvienko M, Torres MJ, Yoder JI (2001a) Transcriptional responses in the hemiparasitic plant Triphysaria versicolor to host plant signals. Plant Physiol 127:272–282
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
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
Mou Z, Fan WH, Dong XN (2003) Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113:935–944
Mower JP, Stefanovic S, Young GJ, Palmer JD (2004) Plant genetics: gene transfer from parasitic to host plants. Nature 432:165–166
Musselman LJ, Dickison WC (1975) The structure and development of the haustorium in parasitic Scrophulariaceae. Bot J Linn Soc 70:183–212
Nester EW, Gordon MP, Kerr A (2005) Agrobacterium tumefaciens: from plant pathology to biotechnology. APS Press, St. Paul, MN
Nickrent DL, Musselman LJ, Riopel JL, Eplee RE (1979) Haustorial initiation and non-host penetration in witchweed (Striga asiatica). Ann Bot 43:233–236
Nwoke F, Okonkwo SNC (1978) Structure and development of the primary haustorium in Alectra vogelii Benth. Ann Bot 42:447–454
O’Brien P (1991) Molecular mechanisms of quinone toxicity. Chem Biol Interact 80:1–41
O’Malley RC, Lynn DG (2000) Expansin message regulation in parasitic angiosperms: marking time in development. Plant Cell 12:1455–1465
Okonkwo SNC (1966) Studies of Striga senegalensis Benth. I. Mode of host-parasite union and haustorial structure. Phytomorphology 16:453–463
Okonkwo SNC, Nwoke FIO (1978) Initiation, development and structure of the primary haustorium in Striga gesnerioides (Scrophulariaceae). Ann Bot 42:455–463
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
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
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
Rich PJ, Grenier C, Ejeta G (2004) Striga resistance in the wild relatives of sorghum. Crop Sci 44:2221–2229
Riopel JL (1983) The biology of parasitic plants: physiological aspects. In: Moore R (ed) Vegetative compatibility. Academic, New York, pp 13–34
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
Riopel J, Musselman L (1979) Experimental initiation of haustoria in Agalinis purpurea. Am J Bot 66:570–575
Riopel JL, Timko MP (1995) Haustorial initiation and differentiation. In: Press MC, Graves JD (eds) Parasitic plants. Chapman and Hall, London, pp 39–79
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
Saunders AR (1933) Studies in phanerogamic parasitism with particular reference to Striga lutea. Sci Bull Union S Afr Dep Agric 128:5–56
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
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
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
Testa B (1995) The metabolism of drugs and other xenobiotics: biochemistry of redox reactions. Academic, New York
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
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
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
Werth C, Riopel JL (1979) A study of the host range of Aureolaria pedicularia (L.) Raf. (Scrophulariaceae). Am Midl Nat 102:300–306
Westwood JH, Yoder JI, Timko MP, dePamphilis CW (2010) The evolution of parasitism in plants. Trends Plant Sci 15:227–235
William CN (1961) Growth and morphogenesis of Striga seedlings. Nature 189:378–381
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
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
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
Yoder JI (1997) A species-specific recognition system directs haustorium development in the parasitic plant Triphysaria (Scrophulariaceae). Planta 202:407–413
Yoder JI (1999) Parasitic plant responses to host plant signals: a model for subterranean plant–plant interactions. Curr Opin Plant Biol 2:65–70
Yoshida S, Maruyama S, Nozaki H, Shirasu K (2010) Horizontal gene transfer by the parasitic plant Striga hermonthica. Science 328:1128
Zeng ZX, Cartwright CH, Lynn DG (1996) Cyclopropyl-p-benzoquinone – a specific organogenesis inhibitor in plants. J Am Chem Soc 118:1233–1234
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
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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
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