Skip to main content

Hemiparasitic Plants: Exploiting Their Host’s Inherent Nature to Talk

  • Chapter
  • First Online:
Plant-Environment Interactions

Abstract

Parasitic plants invade and rob host plants of water, minerals and carbohydrates. Host attachment, invasion and resource acquisition is mediated through a parasite-encoded organ called the haustorium. Since the vast majority of plants don't develop haustoria, it is of interest to understand the genetic mechanisms that provide parasites with this novel organ. Host–parasite signaling has been most extensively investigated in the Orobanchaceae, a family of root parasites that includes some of the world's worst agricultural weeds. The need for host resources varies widely among different Orobanchaceae species. Facultative hemiparasites, essentially autotrophic plants that are able to make haustoria, grow fine without ever attacking a host. In contrast, obligate holoparasites are incapable of photosynthesis and require host attachment soon after germination to survive. While morphologically quite different, all parasitic Orobanchaceae develop haustoria in response to chemical and tactile cues provided by their host plants. This review will focus on host signal recognition by hemiparasites, since they represent the earliest stage in the evolutionary transition from autotrophy to heterotrophy. Parasitic plant–host plant interactions provide an excellent illustration of how plants respond to signals in their environments, and how they in turn alter the environment in which they live.

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 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
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

  • Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827

    Article  PubMed  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. Evol 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 

  • 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 

  • Barkman TJ, Lim S-H, Salleh KM, Nais J (2004) Mitochondrial DNA sequences reveal the photosynthetic relatives of Rafflesia, the world's largest flower. Proc Natl Acad Sci USA 101:787–792

    Article  PubMed  CAS  Google Scholar 

  • Barkman T, McNeal J, Lim S-H, Coat G, Croom H, Young N, dePamphilis C (2007) Mitochondrial DNA suggests at least 11 origins of parasitism in angiosperms and reveals genomic chimerism in parasitic plants. BMC Evol Biol 7:248

    Article  PubMed  Google Scholar 

  • Berner DK, Cardwell KF, Faturoti BO, Ikie FO, Williams OA (1994) Relative roles of wind, crop seeds, and cattle in dispersal of Striga ssp. Plant Dis 78:402–406

    Article  Google Scholar 

  • Birschwilks M, Haupt S, Hofius D, Neumann S (2006) Transfer of phloem-mobile substances from the host plants to the holoparasite Cuscuta sp. J Exp Bot 57:911–921

    Article  PubMed  CAS  Google Scholar 

  • Bommer D, Haberhausen G, Zetsche K (1993) A large deletion in the plastid DNA of the holoparasitic flowering plant Cuscuta reflexa concerning 2 ribosomal proteins (RPL2, RPL23), one transfer RNA (TRNI) and an ORF-2280 homolog. Curr Genet 24:171–176

    Article  PubMed  CAS  Google Scholar 

  • Botanga CJ, Timko MP (2006) Phenetic relationships among different races of Striga gesnerioides (Willd.) Vatke from West Africa. Genome 49:1351–1365

    Article  PubMed  Google Scholar 

  • Bouwmeester HJ, Roux C, Lopez-Raez JA, Becard G (2007) Rhizosphere communication of plants, parasitic plants and AM fungi. Trends Plant Sci 12:224–230

    Article  PubMed  CAS  Google Scholar 

  • Brambilla G, Robbiano L, Cajelli E, Martelli A, Turmolini F, Mazzei M (1988) DNA-damaging and mutagenic properties of 2,6-dimethoxy-1,4-benzoquinone, formed by dimethoprine-nitrite interaction. Int J Clin Pharmacol 244:1011–1015

    CAS  Google Scholar 

  • Bright LJ, Liang Y, Mitchell DM, Harris JM (2005) The LATD gene of Medicago truncatula is required for both nodule and root development. Mol Plant Microbe Interact 18:521–532

    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 

  • Chuang TI, Heckard LR (1991) Generic realignment and synopsis of subtribe Castillejinae (Scrophulariaceae—tribe Pediculareae). Syst Bot 16:644–666

    Article  Google Scholar 

  • Combes C (2001) Parasitism: the ecology and evolution of intimate interactions. University of Chicago Press, Chicago

    Google Scholar 

  • Cook CE, Whichard LP, Wall ME, Egely GH (1966) Germination of witchweed (Striga lutea Lour.): isolation and properties of a potent stimulant. Science 196:1189–1190

    Article  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 

  • Delavault PM, Russo NM, Lusson NA, Thalouarn PA (1996) Organization of the reduced plastid genome of Lathraea clandestina, an achlorophyllous parasitic plant. Physiol Plant V96:674–682

    Article  Google Scholar 

  • dePamphilis CW, Young NN, Wolfe AD (1997) Evolution of plastid gene rps2 in a lineage of hemiparasitic and holoparasitic plants: many losses of photosynthesis and complex patterns of rate variation. Proc Natl Acad Sci USA 93:7367–7372

    Article  Google Scholar 

  • Der JP, Nickrent DL (2008) A molecular phylogeny of Santalaceae (Santalales). Syst Bot 33:107–116

    Article  Google Scholar 

  • Dobzhansky T (1964) Biology, molecular and organismic. Am Zool 4:443–452

    PubMed  CAS  Google Scholar 

  • Dorr I (1997) How Striga parasitizes its host: a TEM and SEM study. Ann Bot 79:463–472

    Article  Google Scholar 

  • Ehleringer JR, Marshall JD (1995) Water relations. In: Press MC, Graves JD (eds) Parasitic plants. Chapman and Hall, London, pp. 124–140

    Google Scholar 

  • Feild TS, Brodribb TJ (2005) A unique mode of parasitism in the conifer coral tree Parasitaxus ustus (Podocarpaceae). Plant Cell Environ 28:1316–1325

    Article  CAS  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 

  • Garth RE (1964) The ecology of Spanish moss (Tillandsia usneoides): its growth and distribution. Ecol 45:470–481

    Article  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

    Google Scholar 

  • Govier RN, Nelson MD, Pate JS (1967) Hemiparasitic nutrition in angiosperms: the transfer of organic compounds from host to Odontites verna (Bell.) Dum. (Scrophulariaceae). New Phytol 66:285–297

    Article  CAS  Google Scholar 

  • Haberhausen G, Valentin K, Zetsche K (1992) Organization and sequence of photosynthetic genes from the plastid genome of the holoparasitic flowering plant Cuscuta reflexa. Mol Gen Genet 232:154–161

    Article  PubMed  CAS  Google Scholar 

  • Handa S, Kinghorn A, Cordell G, Farnsorth N (1983) Plant anticancer agents XXVI. Constituents of Peddiea fischeri. J Nat Prod 46:248–250

    Article  PubMed  CAS  Google Scholar 

  • Harrison MJ (1999) Molecular and cellular aspects of the arbuscular mycorrhizal symbiosis. Ann Rev Plant Phys Plant Mol Biol 50:361–389

    Article  CAS  Google Scholar 

  • Haupt S, Oparka K, Sauer N, Neumann S (2001) Macromolecular trafficking between Nicotiana tabacum and the holoparasite Cuscuta reflexa. J Exp Bot 52:173–177

    Article  PubMed  CAS  Google Scholar 

  • Hawksworth FG, Wiens D (1996) Dwarf mistletoes: biology, pathology, and systematics. United States Department of Agriculture Forest Service, Washington, DC

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Heide-Jørgensen HS, Kuijt J (1993) Epidermal derivatives as xylem elements and transfer cells: a study of the host–parasite interface in two species of Triphysaria (Scrophulariaceae). Protoplasma 174:173–183

    Article  Google Scholar 

  • Heide-Jørgensen HS, Kuijt J (1995) The haustorium of the root parasite Triphysaria (Scrophulariaceae), with special reference to xylem bridge ultrastructure. Am J Bot 82:782–797

    Article  Google Scholar 

  • Hibberd JM, Jeschke WD (2001) Solute flux into parasitic plants. J Exp Bot 52:2043–2049

    Article  PubMed  CAS  Google Scholar 

  • Hull RJ, Leonard OA (1964) Physiological aspects of parasitism in mistletoes (Arceuthobium and Phoradendron). II. The photosynthetic capacity of mistletoe. Plant Physiol 39:1008–1017

    Article  PubMed  CAS  Google Scholar 

  • Humphrey AJ, Beale MH (2006) Strigol: biogenesis and physiological activity. Phytochemistry 67:636–640

    Article  PubMed  CAS  Google Scholar 

  • Jiang F, Jeschke WD, Hartung W, Cameron DD (2008) Does legume nitrogen fixation underpin host quality for the hemiparasitic plant Rhinanthus minor? J Exp Bot 59:917–925

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Jones KM, Kobayashi H, Davies BW, Taga ME, Walker GC (2007) How rhizobial symbionts invade plants: the Sinorhizobium-Medicago model. Nat Rev Microbiol 5:619–633

    Article  PubMed  CAS  Google Scholar 

  • Kim D, Kocz R, Boone L, Keyes WJ, Lynn DG (1998) On becoming a parasite: evaluating the role of wall oxidases in parasitic plant development. Chem Biol 5:103–117

    Article  PubMed  CAS  Google Scholar 

  • Knutson DM (1979) How parasitic seed plants induce disease in other plants. In: Horsfall JG, Cowling EB (eds) Plant disease: an advanced treatise. Academic Press, San Diego, pp 293–312

    Google Scholar 

  • Kohmoto K, Singh US, Singh RP (1995) Pathogenesis and host specificity in plant pathogenic fungi and nematodes. In: Kohmoto K, Singh US, Singh RP (eds) Pathogenesis and host specificity in plant diseases: histopathological, biochemical, genetic and molecular bases, vol. 2. Elsevier, Tarrytown, pp. xxi–xxvii

    Google Scholar 

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

    Google Scholar 

  • Kuijt J (1991) The haustorial interface: what does it tell us? In: Ranson J, Musselman LJ, Worsham AD, Parker C (eds) Proceedings of the Fifth International Symposium of Parasitic Weeds. CIM-MYT, Narobi

    Google Scholar 

  • Leake JR (1994) The biology of myco-heterotrophic ("saprophytic") plants. New Phytol 127:171–216

    Article  Google Scholar 

  • Livingston WH, Brenner ML, Blanchette RA (1984) Altered concentrations of abscisic acid, indole-3-acetic acid zeatin riboside associated with eastern dwarf mistletoe infections on black spruce. In: Hawksworth FG, Scharpf RF (eds) Biology of Dwarf Mistletoes. USDA Forest Service, Fort Collins, pp 53–61

    Google Scholar 

  • Machado MA, Zetsche K (1990) A structural, functional and molecular analysis of plastids of the holoparasites Cuscusta reflexa and Cuscuta europaea. Planta 181:91–96

    Article  CAS  Google Scholar 

  • Malécot V, Nickrent DL (2008) Molecular phylogenetic relationships of Olacaceae and related Santalales. Syst Bot 33:97–106

    Article  Google Scholar 

  • Marshall JD, Ehleringer JR, Schulze ED, Farquhar G (1994) Carbon-isotope composition, gas-exchange and heterotrophy in Australian mistletoes. Funct Ecol 8:237–241

    Article  Google Scholar 

  • Marvier MA (1998) A mixed diet improves performance and herbivore resistance of a parasitic plant. Ecol 79:1272–1280

    Article  Google Scholar 

  • Matusova R, Rani K, Verstappen FWA, Franssen MCR, Beale MH, Bouwmeester HJ (2005) The strigolactone germination stimulants of the plant-parasitic Striga and Orobanche spp. are derived from the carotenoid pathway. Plant Physiol 139:920–934

    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  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  CAS  Google Scholar 

  • Mayer AM (2006) Pathogenesis by fungi and by parasitic plants: similarities and differences. Phytoparasitica 34:3–16

    Article  CAS  Google Scholar 

  • Mendgen K, Deising H (1993) Infection structures of fungal plant pathogens: a cytological and physiological evaluation. New Phytol 124:193–213

    Article  Google Scholar 

  • Morden CW, Wolfe KH, dePamphilis CW, Palmer JD (1991) Plastid translation and transcription genes in a non-photosynthetic plant: intact, missing and pseudo genes. EMBO J 10:3281–3288

    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 (1980) The biology of Striga, Orobanche, and other root parasitic weeds. Ann Rev Phytopath 18:463–489

    Article  Google Scholar 

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

    Google Scholar 

  • Nickrent D (2007) The parasitic plant connection. http://www.parasiticplants.siu.edu/. Cited June 2008

  • Nickrent DL, Duff RJ, Colwell AE, Wolfe AD, Young ND, Steiner KE, dePamphilis CW (1998) Molecular phylogenetic and evolutionary studies of parasitic plants. In: Soltis DE, Soltis PS, Doyle JJ (eds) Molecular systematics of plants II: DNA sequencing. Kluwer, Boston, pp 211–241

    Chapter  Google Scholar 

  • Okonkwo SNC (1966) Studies on Striga senegalensis. II. Translocation of 14 C-labeled photosynthate, urea-14C and sulphur35 between host and parasite. Am J Bot 53:142

    Article  CAS  Google Scholar 

  • Parker C, Riches CR (1993) Parasitic weeds of the world: biology and control. CAB International, Wallingford

    Google Scholar 

  • Pate JS, Kuo J, Davidson NJ (1990) Morphology and anatomy of the haustorium of the root hemiparasite Olax phyllanthi (Olacaceae), with a special reference to the haustorial interface. Ann Bot 65:425–436

    Google Scholar 

  • Pieterse CMJ, Dicke M (2007) Plant interactions with microbes and insects: from molecular mechanisms to ecology. Trends Plant Sci 12:564–569

    Article  PubMed  CAS  Google Scholar 

  • Press MC (1995) Carbon and nitrogen relations. In: Press MC, Graves JD (eds) Parasitic plants. Chapman and Hall, London, pp. 103–124

    Google Scholar 

  • Press MC, Graves JD (eds) (1995) Parasitic plants. Chapman and Hall, London

    Google Scholar 

  • Press MC, Tuohy JM, Stewart GR (1987) Gas exchange characteristics of the Sorghum-Striga host–parasite association. Plant Physiol 84:814–819

    Article  PubMed  CAS  Google Scholar 

  • Press MC, Graves JD, Stewart GR (1990) Physiology of the interaction of angiosperm parasites and their higher plant hosts. Plant Cell Environ 13:91–104

    Article  Google Scholar 

  • Press MC, Whittaker JB (1993) Exploitation of the xylem stream by parasitic organisms. Philos Trans R Soc Lond B Biol Sci 341:101–111

    Article  Google Scholar 

  • Raka MM, Cynthia AG, Anne E, James H, J AD, Giles EDO, Sharon RL (2004) A Ca2+/calmodulin-dependent protein kinase required for symbiotic nodule development: gene identification by transcript-based cloning. Proc Natl Acad Sci USA 101:4701–4705

    Article  Google Scholar 

  • Rank C, Rasmussen LS, Jensen SR, Pierce S, Press MC, Scholes JD (2004) Cytotoxic constituents of Alectra and Striga species. Weed Res 44:265–270

    Article  CAS  Google Scholar 

  • Richardson AO, Palmer JD (2006) Horizontal gene transfer in plants. J Exp Bot 58:1–9

    Article  PubMed  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, vol. 1. CRC, Boca Raton, pp 107–125

    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 

  • Robert S, Simier P, Fer A (1999) Purification and characterization of mannose 6-phosphate reductase, a potential target for the control of Striga hermonthica and Orobanche ramosa. Aust J Plant Physiol 26:233–237

    Article  CAS  Google Scholar 

  • Roney JK, Khatibi PA, Westwood JH (2007) Cross-species translocation of mRNA from host plants into the parasitic plant dodder. Plant Physiol 143:1037–1043

    Article  PubMed  CAS  Google Scholar 

  • Roth C, Rastogi S, Arvestad L, Dittmar K, Light S, Ekman D, Liberles DA (2007) Evolution after gene duplication: models, mechanisms, sequences, systems, and organisms. J Exp Zool 308B:58–73

    Article  CAS  Google Scholar 

  • Scholes JD, Press MC (2008) Striga infestation of cereal crops: an unsolved problem in resource limited agriculture. Curr Opin Plant Biol 11:180–186

    Article  PubMed  Google Scholar 

  • Shah N, Smirnoff N, Stewart G (1987) Photosynthesis and stomatal characteristics of Striga hermonthica in relation to its parasitic habit. Physiol Plant 69:699–703

    Article  Google Scholar 

  • Shen H, Ye W, Hong L, Huang H, Wang Z, Deng X, Yang Q, Xu Z (2006) Progress in parasitic plant biology: host selection and nutrient transfer. Plant Biol 8:175–185

    Article  PubMed  CAS  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 

  • Tank DC, Beardsley PM, Kelchner SA, Olmstead RG (2006) Review of the systematics of Scrophulariaceae s.l and their current disposition. Aust System Bot 19:289–307

    Article  Google Scholar 

  • Tennakoon KU, Pate JS, Stewart GR (1997) Haustorium-related uptake and metabolism of host xylem solutes by the root hemiparasitic shrub Santalum acuminatum (R. Br.) ADC (Santalaceae). Ann Bot 80:257–264

    Article  CAS  Google Scholar 

  • Tennakoon KU, Bolin JF, Musselman LJ, Maass E (2007) Structural attributes of the hypogeous holoparasite Hydnora triceps Drege & Meyer (Hydnoraceae). Am J Bot 94:1439–1449

    Article  PubMed  Google Scholar 

  • Testa B (1995) The metabolism of drugs and other xenobiotics. Academic Press, New York

    Google Scholar 

  • Thurman LD (1966) Genecological studies in Orthocarpus subgenus Triphysaria. University of California, Berkeley

    Google Scholar 

  • Tomilov AA, Tomilova NB, Wroblewski T, Michelmore R, Yoder JI (2008) Trans-specific gene silencing between host and parasitic plants. Plant J 56(3):389–397

    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 24:24

    Article  Google Scholar 

  • Visser J, Dorr I (1987) The haustorium. In: Musselman LJ (ed) Parasitic weeds in agriculture, vol. 1. CRC, Boca Raton, pp 91–106

    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 

  • Young ND, Steiner KE, dePamphilis CW (1999) The evolution of parasitism in Scrophulariaceae/Orobanchaceae: plastid gene sequences refute an evolutionary transition series. Ann Mo Bot Gard V86:876–893

    Article  Google Scholar 

  • Zaneveld JR, Nemergut DR, Knight R (2008) Are all horizontal gene transfers created equal? Prospects for mechanism-based studies of HGT patterns. Microbiology 154:1–15

    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 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Yoder, J.I., Gunathilake, P., Jamison-McClung, D. (2009). Hemiparasitic Plants: Exploiting Their Host’s Inherent Nature to Talk. In: Balu¿ka, F. (eds) Plant-Environment Interactions. Signaling and Communication in Plants. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-89230-4_5

Download citation

Publish with us

Policies and ethics