WO2007121978A1 - Substance de lutte contre la formation d'haustories utilisée en tant que produit phytosanitaire contre des phytoparasites - Google Patents

Substance de lutte contre la formation d'haustories utilisée en tant que produit phytosanitaire contre des phytoparasites Download PDF

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Publication number
WO2007121978A1
WO2007121978A1 PCT/EP2007/003556 EP2007003556W WO2007121978A1 WO 2007121978 A1 WO2007121978 A1 WO 2007121978A1 EP 2007003556 W EP2007003556 W EP 2007003556W WO 2007121978 A1 WO2007121978 A1 WO 2007121978A1
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Prior art keywords
nucleic acid
polypeptide
plant
spp
sequence
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PCT/EP2007/003556
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German (de)
English (en)
Inventor
Ralf Kaldenhoff
Markus Albert
Marc Bleischwitz
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Technische Universität Darmstadt
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Publication of WO2007121978A1 publication Critical patent/WO2007121978A1/fr

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    • C—CHEMISTRY; METALLURGY
    • C12—BIOCHEMISTRY; BEER; SPIRITS; WINE; VINEGAR; MICROBIOLOGY; ENZYMOLOGY; MUTATION OR GENETIC ENGINEERING
    • C12N—MICROORGANISMS OR ENZYMES; COMPOSITIONS THEREOF; PROPAGATING, PRESERVING, OR MAINTAINING MICROORGANISMS; MUTATION OR GENETIC ENGINEERING; CULTURE MEDIA
    • C12N15/00—Mutation or genetic engineering; DNA or RNA concerning genetic engineering, vectors, e.g. plasmids, or their isolation, preparation or purification; Use of hosts therefor
    • C12N15/09—Recombinant DNA-technology
    • C12N15/63—Introduction of foreign genetic material using vectors; Vectors; Use of hosts therefor; Regulation of expression
    • C12N15/79—Vectors or expression systems specially adapted for eukaryotic hosts
    • C12N15/82—Vectors or expression systems specially adapted for eukaryotic hosts for plant cells, e.g. plant artificial chromosomes (PACs)
    • C12N15/8241—Phenotypically and genetically modified plants via recombinant DNA technology
    • C12N15/8261—Phenotypically and genetically modified plants via recombinant DNA technology with agronomic (input) traits, e.g. crop yield
    • C12N15/8271—Phenotypically and genetically modified plants via recombinant DNA technology with agronomic (input) traits, e.g. crop yield for stress resistance, e.g. heavy metal resistance
    • C12N15/8279—Phenotypically and genetically modified plants via recombinant DNA technology with agronomic (input) traits, e.g. crop yield for stress resistance, e.g. heavy metal resistance for biotic stress resistance, pathogen resistance, disease resistance
    • C—CHEMISTRY; METALLURGY
    • C12—BIOCHEMISTRY; BEER; SPIRITS; WINE; VINEGAR; MICROBIOLOGY; ENZYMOLOGY; MUTATION OR GENETIC ENGINEERING
    • C12N—MICROORGANISMS OR ENZYMES; COMPOSITIONS THEREOF; PROPAGATING, PRESERVING, OR MAINTAINING MICROORGANISMS; MUTATION OR GENETIC ENGINEERING; CULTURE MEDIA
    • C12N9/00—Enzymes; Proenzymes; Compositions thereof; Processes for preparing, activating, inhibiting, separating or purifying enzymes
    • C12N9/14—Hydrolases (3)
    • C12N9/48—Hydrolases (3) acting on peptide bonds (3.4)
    • C12N9/50—Proteinases, e.g. Endopeptidases (3.4.21-3.4.25)
    • C12N9/64—Proteinases, e.g. Endopeptidases (3.4.21-3.4.25) derived from animal tissue
    • C12N9/6421—Proteinases, e.g. Endopeptidases (3.4.21-3.4.25) derived from animal tissue from mammals
    • C12N9/6472—Cysteine endopeptidases (3.4.22)

Definitions

  • the present invention relates to a peptide inhibitor of a plant cysteine protease which inhibits the formation of haustoria in plant pathogens and its use as a plant protection agent, in particular in tomato or soybean.
  • the family Cuscutaceae (sometimes this family is also counted among the Convolvulaceae) includes about 150 species of the genus Cuscuta, all of which live parasitically on other angiosperms. All Cuscuta A ⁇ en consist of a sinuous shoot, have no roots and only rudimentary, flaky leaves. In local latitudes, Cuscuta europapea, also called devil's twine or spring-silk, is native to and above all found on river meadows, whereby the nettle usually serves as a host plant.
  • haustoria Cwscttta plants make contact with the vascular system of the host plants and deprive them of organic and inorganic nutrients. But these haustoria are not just nutrients.
  • Cuscuta also serves as an effective vector for the delivery of various viruses, and the transfer of RNAs or RNA-protein complexes can not be ruled out.
  • Cuscuta reflexa infects almost every plant and deprives the host plants of important nutrients, which can lead to the death of the infected plants. Whole fields of crops can be destroyed in this way. Especially in soybean and tomato growing in America and Southeast Asia, this has devastating consequences. Since Cuscuta reflexa is a higher plant, it is particularly difficult to effectively combat the parasites without harming the crops.
  • ERSAT ⁇ SHEET (RULE 26) Hand removed In case of larger infestation, the field may be burned down to prevent an epidemic. (Source: http://www.ipm.ucdavis.edulPMGIPESTNOTESlpn7496.html) As an alternative, one uses the spray glyphosate ("RoundUp” ®)
  • haustoria The development of haustoria is vital to Cuscuta's survival and is the key to successful infection. Cellular factors play an essential role in the development of haustoria.
  • Nadler-Hassar et al. (Nadler-Hassar T, Goldshmidt A, Rubin B, Wolf S. Glyphosate inhibits the translocation of green fluorescent protein and sucrose from a transgenic tobacco host to Cuscuta campestris Yunk Planta 2004 Sep; 219 (5): 790-6. Epub 2004 Jun 2.) describe the effect of glyphosate on Cuscuta campestris on tobacco.
  • Torres et al. (Torres MJ, Tomilov AA, Tomilova N, Reagan RL, Yoder Jsc, Pscroph, a parasitic EST database enriched for parasite-associated transcripts, BMC Plant Biol. 2005 Nov 16; 5: 24.) Describe a haustoria-relevant EST database ,
  • Tada et al. (Tada Y, Wakasugi T, Nishikawa A, Furuhashi K, Yamada K) Developmental Regulation of a Low-Molecular-weight Heat Shock Protein During Fodus formation in the seedling of a holoparasitic plant, Cuscuta japonica., Plant Cell Physiol. 2000 Dec; 41 (12): 1373-80.) Describe the identification of a gene involved in the formation of haustoria in Cuscuta japonica.
  • the sequence number AF 138265 relates to a particular cysteine protease (papain-like cysteine proteinase isoform II) from the sweet potato (Ipomoea batatas). This was deposited on March 26, 1999 in the database.
  • the sequence number Q9M7D5 IPOBA also relates to a particular cysteine protease. This was deposited in the database in October 2000.
  • US 6,451,604 also describes a particular cysteine protease (Sequence 165).
  • WO 02/22675 relates to a particular cysteine protease (Sequence 500) from Arabidopsis thaliana.
  • US 4,915,726 relates to a method of controlling Cuscuta, wherein the plant is sprayed with a fungal culture as a mycoherbicide.
  • Valueva and Mosolov (Roe of inhibitors of proteolytic enzymes in plant defense against phytopathogenic microorganisms, Biochemistry (Moses), 2004 Nov; 69 (l): 1305-9) describe various uses of proteinases and their inhibitors.
  • this object is achieved by a polypeptide of a cysteine protease comprising an inhibitor peptide according to SEQ ID NO: 1 or a peptide sequence having at least 80% and preferably 90% amino acid identity to SEQ ID NO: 1
  • a cysteine protease comprising an inhibitor peptide having at least 95% amino acid identity to SEQ ID NO: 1.
  • Peptides preferred according to the invention comprise the inhibitor peptide according to SEQ ID No. 2, optionally with an N- or C-terminal amino acid extension, preferably with a length of 5, more preferably 10, even more preferably 20, 50 or 100 amino acids in length, either from a corresponding protease or as a fusion protein.
  • Components of the fusion protein may be, for example, enzyme labels.
  • the peptide of the invention may be of any length as long as the peptide inhibits haustoria formation under appropriate conditions. However, preference is given to inhibitor peptides according to the invention which do not comprise the complete protease sequence.
  • a polypeptide according to the invention according to SEQ ID No. 2 is particularly preferred.
  • the peptide according to the invention can also be its homologue or orthologue of the peptide of SEQ ID No. 1 or SEQ ID No. 2.
  • the present invention provides a way of preventing parasitic infestation of host plants by house-producing plant pathogens, preferably Cuscuta, pathogenic fungi and particularly preferably C. reflexa, and to prevent plants which have already been attacked by parasites. free.
  • house-producing plant pathogens preferably Cuscuta, pathogenic fungi and particularly preferably C. reflexa
  • a harmless peptide according to the invention in an aqueous solution, for example, which is also biodegradable, penetration of infectious organs of the parasite (haustoria) is prevented or dissolves the parasite from the treated plant. In this way, a spread of the parasite on agricultural land is suppressed.
  • the proteinase according to the invention (SEQ ID NO: 2) is produced by the parasite as a so-called Pra-Pro protein and then secreted by means of pre-peptide to the outside in the vicinity of the potential host.
  • the pro-peptide which acts as an inhibitor of the proteinase function
  • the actual proteinase is activated. If the proteinase is inhibited, this prevents the successful infection and prevents the spread of the parasite.
  • EP 1,637,607 describes promoters for the activation of plant genes after infections with pathogens, such as bacteria, viruses, fungi, unicellulars.
  • the promoters in question should be able to regulate the transcription of specific genes of the host plant by interaction with pathogens or elicitors.
  • a peptide from the parasite Cuscuta is used to repel the parasite.
  • a reaction of the host plant to the infection with the pathogen is not provided.
  • an interaction of host and parasite by establishing chimeric cell walls should just be prevented.
  • the method in EP 1,637,607 also refers to the genes of the host for the identification of genes induced by pathogens.
  • cysteine protease described in the present patent application, however, differs fundamentally.
  • a parasite-specific protease with a Parasite-specific inhibitor is a parasite-specific infection mechanism, the Hau- storien Struktur be prevented.
  • the invention is a cysteine proteinase inhibitor, a peptide from the parasite Cuscuta reflexa, which is intended to protect crops.
  • This peptide can be easily prepared by common biotechnological methods. By spraying this peptide on host plants for the parasite C. reflexa can be successfully prevent parasitization.
  • the present invention is innovative for several reasons: it is easy to manufacture, easy to use, and environmentally friendly.
  • polypeptide of the invention may be characterized by being synthetically produced. Corresponding methods are well known to those skilled in the art and described in the literature. Furthermore, the peptides according to the invention can also be present as retro-inverse peptides or peptidomimetics, which differ in particular from the structure of the peptide backbone of conventional peptides.
  • the invention also relates to a method for optimizing an inhibitor peptide according to the invention, in which the inhibitor peptide is modified in its amino acid sequence by standard methods (eg by conservative or non-conservative amino acid substitutions) and the peptide thus modified is examined for its properties which may normally include effectiveness in inhibiting skin aorta and stability in compositions, but also reduced toxicity or degradability.
  • Correspondingly modified inhibitor peptides are also included in the present invention and also have at least 80% and preferably 90% amino acid identity to SEQ ID NO: 1.
  • a further aspect of the present invention relates to a nucleic acid which codes for a polypeptide according to the invention.
  • the nucleic acid is characterized in that it is a DNA, RNA, mRNA, cDNA, CNA, PNA, preferably a DNA, in particular a double-stranded DNA having a length of at least 24 nucleotides.
  • the nucleic acids according to the invention can also be longer.
  • a nucleic acid according to the invention characterized in that the sequence of the nucleic acid has at least one intron and / or one polyA sequence.
  • Particularly preferred is a nucleic acid according to the invention in the form of its complementary "antisense" sequence.
  • the nucleic acid may be characterized in that it has been produced synthetically. Corresponding methods are well known to those skilled in the art and described in the literature.
  • a further aspect of the present invention then relates to a vector, preferably in the form of a plasmid, shuttle vector, phagemid, cosmid, expression vector, retroviral vector, adenoviral vector or particle and / or gene-therapeutically active vector comprising a nucleic acid according to the invention.
  • Yet another aspect of the present invention relates to a method of producing an antibody directed against a polypeptide of the invention, preferably a polyclonal or monoclonal antibody, for inhibiting a polypeptide of the invention comprising an antibody-producing organism with a polypeptide of the invention or portions thereof having at least 6 amino acids, preferably is immunized with at least 8 amino acids, in particular with at least 12 amino acids.
  • These antibodies can serve as tools in the study of the function of the peptides of the invention.
  • Yet another aspect of the present invention relates to an antibody, particularly monoclonal antibody, prepared as above directed against a polypeptide of the invention.
  • Antibody fragments can also be made, such as recombinant scFv antibody fragments or Fab.
  • the object is achieved by a process for the preparation of a crop protection composition
  • a process for the preparation of a crop protection composition comprising mixing a polypeptide according to the invention with a suitable carrier.
  • the carrier can be an aqueous solution, a combination with a conventional crop protection agent or a cell lysate.
  • a crop protection composition prepared according to the invention comprising a polypeptide according to the invention, a nucleic acid according to the invention and / or an antibody according to the invention, optionally with a suitable carrier as above.
  • the object is achieved by a method for producing a transgenic plant comprising transformation of a plant cell with a nucleic acid according to the invention.
  • the cell is transformed with an expression construct to express a polypeptide of the invention.
  • Preferred is a method wherein the nucleic acid is preceded by an export sequence, so that the peptide is exported from the cell.
  • the polypeptide By expression of the polypeptide by the host plant itself, it is capable of directly repelling the parasite. Preference is given to two possibilities: a) integration of the nucleic acid sequence (s) encoding the polypeptide of the invention into the genome of the host plant, and b) integration of the nucleic acid sequence (s) encoding the polypeptide of the invention into the genome of the host plant including an upstream export sequence such that the peptide is brought outside and in direct contact with the parasite.
  • a preferred export sequence is the presequence of the cysteine protease (AS 1 to 31 of SEQ ID NO: 2).
  • the object is achieved by a transgenic plant produced by a method according to the invention as above.
  • the transgenic plants may be all plants which are infested by haustoria-producing plant pathogens, but especially plants selected from tomato (Solanum lycopersicum L.), soybean ⁇ Glycine max (L.)), sugar beet (Beta vulgaris), alfalfa ( Alfalfa, Medicago sativa), clover (Trifolium spp.), Wine (Vitis spp.), Red pepper (Capsicum spp.), Onion (Allium cepa), broad bean (Viciafaba), lettuce (Lactuca spp.), Spinach (Spinacia spp .), Bonsai tree and citrus plant.
  • the object is achieved by a method for controlling haustoria-producing plant pathogens comprising applying a crop protection composition as above to a plant.
  • a crop protection composition as above to a plant.
  • the inhibitor peptide according to the invention preferably the propeptide (PIN, SEQ ID NO: 1) derived from the precursor sequence of the cysteine proteinase, e.g. produced in E. coli and can either be purified or even applied in E. coli lysate, the formation of haustoria can be specifically prevented.
  • cysteine proteinase inhibitor peptides of the invention may also be present in the composition according to the invention.
  • the method according to the invention for controlling haustoria-producing plant pathogens can in principle be used for all plant pathogens forming haustoria since it is assumed that the present cysteine proteinase inhibits Tor peptides represent a central target for Haustorien Struktur, since the effectiveness was in the experiments carried out in the invention at 100%. Further preferred is an inventive method for controlling haustoria-producing plant pathogens, wherein the plant pathogens are selected from Cuscuta, pathogenic fungi, rust fungi, mildew and parasites of the family Orobranchaceae.
  • the plants to be treated are all plants which are attacked by haustoria-producing plant pathogens, but especially plants such as tomatoes (Solarium lycospersicum L.), soybeans (Glycine max (L.)), sugar beets (Beta vulgaris), alfalfa (Alfalfa , Medicago sativa), clover (Trifolium spp.), Wine (Vitis spp.), Paprika (Capsicum spp.), Onion (Allium cepa), broad beans (Vicia faba), lettuce (Lactuca spp.), Spinach (Spinacia spp .), Bonai trees and citrus plants.
  • tomatoes Small lycospersicum L.
  • soybeans Glycine max (L.)
  • sugar beets Beta vulgaris
  • alfalfa Alfalfa
  • Medicago sativa Medicago sativa
  • clover Trifolium spp.
  • Bonsai trees are understood to mean, in particular, all woody, small-leaved (or small-noble) tree and shrub species, whereby pine trees, junipers, maples, Asian elm species, azaleas, fruit trees such as cultivated apple or Japanese apricot are traditionally used, but also small-leaved maple species - among them the red-leaved Japanese maple varieties - spruce and beech.
  • Particularly preferred is a method for controlling haustoria-producing plant pathogens wherein the application of the peptides of the invention and / or the composition is carried out by spraying on the plant.
  • a still further aspect of the present invention relates to the use of a erf ⁇ ndungswashen peptide, a nucleic acid according to the invention and / or an antibody of the invention for controlling haustoria-producing plant pathogens as already explained above.
  • a way is shown, which prevents parasitic infestation of host plants by preferably C. reflexa and frees already infected plants from the parasite.
  • a non-hazardous peptide for example in an aqueous solution that is also biodegradable, infiltrating infection organs of the parasite, prevents or dissolves the parasite of the treated plant. In this way, a spread of the parasite on agricultural land is suppressed.
  • SEQ ID NO: 1 The amino acid sequence of the propeptide according to the invention (inhibitor sequence) from C. reflexa.
  • SEQ ID NO: 2 The amino acid sequence of the entire inventive cysteine proteinase from C. reflexa.
  • SEQ ID NO: 3 The cDNA sequence according to the invention of the entire cysteine proteinase from C. reflexa.
  • SEQ ID NO: 4 The cDNA sequence according to the invention of the propeptide (inhibitor sequence).
  • FIG. 1 shows the effect of the inhibitor pro-peptide according to the invention.
  • A normal, unaffected infestation
  • B effect of the inhibitor pro-peptide according to the invention 7 days after administration.
  • FIG. 2 a schematic representation of the Gateway® vector used, showing the Rekombinationsort (dashed lined). At the 5'-end are two 35S promoters. The meaning of the abbreviations: attR: attachment site, Cm r : chloramphenicol resistance, ccdB: "killer gene” (the gene product inhibits the helicase of the cell), nos T: transcriptional stop, Hyg r : hygromycin resistance. The vector also contains kanamycin resistance (not shown).
  • a cDNA library in the scope of about 7000 cDNA clones of the parasite Cuscuta was created. Specifically, tissue from Prehau storien and haustoria used to produce the cDNA library. The parasitic cDNA clones were plated in duplicate on "microarray chips.” Two identical “chips” were hybridized with two different cDNA probes, one with total pre-mammorial and haustorial tissue RNA as template, and the other with total RNA were synthesized from Cuscuta shoot as a template. In this way, so far 2000 cDNA clones have been screened differentially for cDNAs whose genes are induced in haustoria development, ie during infection in the parasite Cuscuta reflexa.
  • the cDNA sequence according to the invention of the entire cysteine proteinase (SEQ ID NO: 3) is:
  • the cDNA sequence of the propeptide (inhibitor sequence) (SEQ ID NO: 4) according to the invention is:
  • amino acid sequence of the polypeptide of the invention (protease sequence) (SEQ ID NO: 2) is (starting methionine underlined):
  • amino acid sequence of the propeptide (inhibitor sequence) (SEQ ID NO: 1) according to the invention is:
  • FIG. 1 Examples of the effect of the pro-peptide are shown in FIG. 1. Left (A) shows the normal unaffected infestation, in the right-hand diagram (B) the effect of the pro-peptide 7 days after application. These results were obtained in 100% of the cases.
  • the constructs were made using Gateway® technology (Invitrogen, U.S.A.). This method is based on the recombination of the construct into the vector, using the site-specific recombination sites of the phage lambda instead of "conventional" ligation using endonuclease and ligase. After recombination, the propeptide is located at the 3 'end of two 35S promoters (FIG. 2) which constitutively express the gene.
  • Agrobacteria (GV3101) were incubated overnight at 28 ° C and 200 rpm in 3 ml 2YT-
  • leaf discs from approx. 6 weeks old tobacco leaves were punched out with a cork borer (0 0.8 cm).
  • the leaf discs were sterilized in 2% sodium hypochlorite solution.
  • To transform the leaf cells with the construct the leaf discs were transferred to the bacterial suspension and incubated for 5 min. Thereafter, the leaf discs were placed on an absorbent material to remove excess fluid. Subsequently, the leaf discs were transferred to co-culture medium (composition see below) and incubated in a climatic cabinet for 2 days at 25 ° C and 16 h light (50-60 ⁇ mol / m 2 s).
  • the discs were transferred to selection medium (composition: see above). After incubation for 1 week at the above ratios, the leaf discs were divided into four parts and incubated for a further three weeks on selection medium. After about three weeks, shoots formed, these were cut off at the base when they had reached a length of 5 - 10 mm and transferred to root medium (composition: see above). After the roots had formed roots, they were removed from the agar and planted in a mixture of soil, perlite and macrolite and covered with a transparent foil for 3-7 days. The period of regeneration to the rooted plant was two months. Six more weeks passed until flowering.
  • Co-culture medium 1 x MS (Murashige & Skoge) micro- and
  • Root medium 1 x MS (Murashige & Skoge) micro and macro elements
  • NAA naphthylacetic acid

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Abstract

La présente invention concerne un inhibiteur peptidique d'une cystéine protéase végétale, qui inhibe la formation d'haustories par des organismes phytopathogènes, et l'utilisation dudit inhibiteur en tant que produit phytosanitaire, en particulier pour la tomate ou le soja.
PCT/EP2007/003556 2006-04-21 2007-04-23 Substance de lutte contre la formation d'haustories utilisée en tant que produit phytosanitaire contre des phytoparasites WO2007121978A1 (fr)

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DE102006018583.8 2006-04-21
DE102006018583.8A DE102006018583B4 (de) 2006-04-21 2006-04-21 Abwehrstoff gegen die Bildung von Haustorien als Pflanzenschutzmittel gegen Pflanzenparasiten

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Citations (3)

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WO2002094008A2 (fr) * 2001-01-26 2002-11-28 Virginia Tech Intellectual Properties, Inc. Plantes transgeniques protegees contre des plantes parasites
US20030082724A1 (en) * 1999-06-04 2003-05-01 Genesis Research And Development Corporation Limited Compositions affecting programmed cell death and their use in the modification of plant development
WO2005030967A2 (fr) * 2003-09-25 2005-04-07 Pioneer Hi-Bred International, Inc. Inhibiteurs de la cystatine proteinase de plantes de culture, et son procede d'utilisation

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ATE542907T1 (de) * 1998-11-12 2012-02-15 Max Planck Gesellschaft Chimäre promotoren, befähigt zur vermittlung der genexpression in pflanzen durch pathogeninfektion und deren anwendungen

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US20030082724A1 (en) * 1999-06-04 2003-05-01 Genesis Research And Development Corporation Limited Compositions affecting programmed cell death and their use in the modification of plant development
WO2002094008A2 (fr) * 2001-01-26 2002-11-28 Virginia Tech Intellectual Properties, Inc. Plantes transgeniques protegees contre des plantes parasites
WO2005030967A2 (fr) * 2003-09-25 2005-04-07 Pioneer Hi-Bred International, Inc. Inhibiteurs de la cystatine proteinase de plantes de culture, et son procede d'utilisation

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ALBERT, MARKUS: "Studien zur Interaktion des pflanzlichen Parasiten Cuscuta reflexa mit dem inkompatiblen Wirt Lycopersicon esculentum", 2005, TU DARMSTADT, FACHBEREICH BIOLOGIE, DARMSTADT, XP002449793 *
DIEGO RUBIALES ET AL: "Screening techniques and sources of resistance against parasitic weeds in grain legumes", EUPHYTICA, KLUWER ACADEMIC PUBLISHERS, DO, vol. 147, no. 1-2, 1 January 2006 (2006-01-01), pages 187 - 199, XP019395492, ISSN: 1573-5060 *
HAQ S K ET AL: "Protein proteinase inhibitor genes in combat against insects, pests, and pathogens: natural and engineered phytoprotection", ARCHIVES OF BIOCHEMISTRY AND BIOPHYSICS, NEW YORK, US, US, vol. 431, no. 1, 1 November 2004 (2004-11-01), pages 145 - 159, XP004581268, ISSN: 0003-9861 *
HUANG D J ET AL: "Expression and function of a cysteine proteinase cDNA from sweet potato (Ipomoea batatas [L.] Lam 'Tainong 57') storage roots", PLANT SCIENCE, LIMERICK, IE, vol. 169, no. 2, August 2005 (2005-08-01), pages 423 - 431, XP004965462, ISSN: 0168-9452 *
KOSKELA TANJA ET AL: "Resistance and tolerance in a host plant-holoparasitic plant interaction: Genetic variation and costs", EVOLUTION, vol. 56, no. 5, May 2002 (2002-05-01), pages 899 - 908, XP002449786, ISSN: 0014-3820 *
PARKER C: "PROTECTION OF CROPS AGAINST PARASITIC WEEDS", CROP PROTECTION, vol. 10, no. 1, 1991, pages 6 - 22, XP002449785, ISSN: 0261-2194 *
PECHAN T ET AL: "A unique 33-kD cysteine proteinase accumulates in response to larval feeding in maize genotypes resistant to fall armyworm and other Lepidoptera", PLANT CELL, AMERICAN SOCIETY OF PLANT PHYSIOLOGISTS, ROCKVILLE, MD, US, vol. 12, no. 7, July 2000 (2000-07-01), pages 1031 - 1040, XP002320387, ISSN: 1040-4651 *
SINGH ARCHANA ET AL: "Incompatibility of Cuscuta haustoria with the resistant hosts-Ipomoea batatas L. and Lycopersicon esculentum Mill", JOURNAL OF PLANT PHYSIOLOGY, vol. 150, no. 5, 1997, pages 592 - 596, XP008083413, ISSN: 0176-1617 *

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