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1.
J Chem Ecol ; 41(1): 52-8, 2015 Jan.
Article in English | MEDLINE | ID: mdl-25563984

ABSTRACT

During insect feeding, a complex interaction takes place at the feeding site, with plants deciphering molecular information associated with the feeding herbivore, resulting in the upregulation of the appropriate defenses, and the herbivore avoiding or preventing these defenses from taking effect. Whiteflies can feed on plants without causing significant damage to mesophyll cells, making their detection extra challenging for the plant. However, whiteflies secrete honeydew that ends up on the plant surface at the feeding site and on distal plant parts below the feeding site. We reasoned that this honeydew, since it is largely of plant origin, may contain molecular information that alerts the plant, and we focused on the defense hormone salicylic acid (SA). First, we analyzed phloem sap from tomato plants, on which the whiteflies are feeding, and found that it contained salicylic acid (SA). Subsequently, we determined that in honeydew more than 80% of SA was converted to its glycoside (SAG). When whiteflies were allowed to feed from an artificial diet spiked with labeled SA, labeled SAG also was produced. However, manually depositing honeydew on undamaged plants resulted still in a significant increase in endogenous free SA. Accordingly, transcript levels of PR1a, an SA marker gene, increased whereas those of PI-II, a jasmonate marker gene, decreased. Our results indicate that whiteflies manipulate the SA levels within their secretions, thus influencing the defense responses in those plant parts that come into contact with honeydew.


Subject(s)
Animal Nutritional Physiological Phenomena , Hemiptera/physiology , Salicylic Acid/metabolism , Solanum lycopersicum/physiology , Animals , Body Fluids/metabolism , Gene Expression Regulation, Plant , Glycosylation , Herbivory , Solanum lycopersicum/chemistry , Solanum lycopersicum/genetics , Phloem/chemistry
2.
Front Plant Sci ; 4: 222, 2013.
Article in English | MEDLINE | ID: mdl-23818892

ABSTRACT

Plants and herbivores have co-evolved in their natural habitats for about 350 million years, but since the domestication of crops, plant resistance against insects has taken a different turn. With the onset of monoculture-driven modern agriculture, selective pressure on insects to overcome resistances has dramatically increased. Therefore plant breeders have resorted to high-tech tools to continuously create new insect-resistant crops. Efforts in the past 30 years have resulted in elucidation of mechanisms of many effective plant defenses against insect herbivores. Here, we critically appraise these efforts and - with a focus on sap-sucking insects - discuss how these findings have contributed to herbivore-resistant crops. Moreover, in this review we try to assess where future challenges and opportunities lay ahead. Of particular importance will be a mandatory reduction in systemic pesticide usage and thus a greater reliance on alternative methods, such as improved plant genetics for plant resistance to insect herbivores.

3.
Proc Natl Acad Sci U S A ; 109(49): 20124-9, 2012 Dec 04.
Article in English | MEDLINE | ID: mdl-23169639

ABSTRACT

Tomato breeding has been tremendously efficient in increasing fruit quality and quantity but did not focus on improving herbivore resistance. The biosynthetic pathway for the production of 7-epizingiberene in a wild tomato was introduced into a cultivated greenhouse variety with the aim to obtain herbivore resistance. 7-Epizingiberene is a specific sesquiterpene with toxic and repellent properties that is produced and stored in glandular trichomes. We identified 7-epizingiberene synthase (ShZIS) that belongs to a new class of sesquiterpene synthases, exclusively using Z-Z-farnesyl-diphosphate (zFPP) in plastids, probably arisen through neo-functionalization of a common ancestor. Expression of the ShZIS and zFPP synthases in the glandular trichomes of cultivated tomato resulted in the production of 7-epizingiberene. These tomatoes gained resistance to several herbivores that are pests of tomato. Hence, introduction of this sesquiterpene biosynthetic pathway into cultivated tomatoes resulted in improved herbivore resistance.


Subject(s)
Biosynthetic Pathways/genetics , Herbivory/immunology , Metabolic Engineering/methods , Sesquiterpenes/immunology , Solanum lycopersicum/immunology , Alkyl and Aryl Transferases/genetics , Alkyl and Aryl Transferases/metabolism , Analysis of Variance , Animals , Breeding/methods , Cloning, Molecular , Feeding Behavior/physiology , Gas Chromatography-Mass Spectrometry , Hemiptera/physiology , Solanum lycopersicum/genetics , Solanum lycopersicum/parasitology , Monocyclic Sesquiterpenes , Polyisoprenyl Phosphates , Real-Time Polymerase Chain Reaction , Sesquiterpenes/metabolism , Tetranychidae/physiology
4.
Plant Cell Environ ; 34(12): 2159-71, 2011 Dec.
Article in English | MEDLINE | ID: mdl-21883286

ABSTRACT

Jasmonate signalling plays a central role in activating the plethora of responses that are elicited by herbivory. Solanum nigrum plants silenced in the expression of genes involved in jasmonic acid biosynthesis (irlox3), conjugation (irjar4) and perception (ircoi1) were used to study the function of these genes in the field and in the regulation of transcriptional and metabolic responses. In the field, damage from Noctuidea larvae was four- to fivefold higher on irlox3 and ircoi1 than on wild-type (WT) plants, whereas damage to irjar4 plants was similar to WT levels. Damage rates reflected plant survival rates; fewer irlox3 (78%) and ircoi1 (22%) plants survived compared with irjar4 and WT plants of which all plants survived. Gene expression profiling in leaves 3 h after simulated herbivory revealed differential regulation of ∼700 genes in irlox3 and ircoi1 plants but of only six genes in irjar4 compared with WT plants. Surprisingly, transcriptional responses were not reflected in metabolomic responses; 48 h after simulated herbivory, irjar4 plants showed a 50% overlap in their metabolic profile with ircoi1 plants. Together, these results reveal that SnJAR4 does not play a direct role in herbivore defence, but suggests that SnJAR4 is involved in responses other than those to herbivory.


Subject(s)
Cyclopentanes/metabolism , Gene Expression Regulation, Plant , Herbivory , Isoleucine/analogs & derivatives , Plant Growth Regulators/metabolism , Signal Transduction , Solanum nigrum/metabolism , Animals , Gene Expression Profiling , Gene Silencing , Isoleucine/metabolism , Larva , Manduca , Metabolome , Oligonucleotide Array Sequence Analysis , Plants, Genetically Modified/genetics , Plants, Genetically Modified/metabolism , Solanum nigrum/genetics , Transcriptome
5.
Trends Plant Sci ; 16(6): 294-9, 2011 Jun.
Article in English | MEDLINE | ID: mdl-21354852

ABSTRACT

The recognition of insect and pathogen attack requires the plant's ability to perceive chemical cues generated by the attacker. In contrast to the recognition of microbe-associated molecular patterns and effectors, little is known about the molecular recognition of herbivore-associated elicitors (HAEs) and the signaling mechanisms operating in plants after their perception. HAE perception depends strongly on the natural history of both plants and insects and it is therefore expected that many of the responses induced by different HAEs are specific to the species involved in the interaction. The interaction between Nicotiana attenuata and the specialist lepidopteran Manduca sexta presents a relevant biological system to understand HAE perception and signal transduction systems in plants.


Subject(s)
Glutamine/analogs & derivatives , Nicotiana/metabolism , Plant Leaves/metabolism , Signal Transduction , alpha-Linolenic Acid/analogs & derivatives , Animals , Cyclopentanes/metabolism , Feeding Behavior , Gene Expression Regulation, Plant , Genes, Plant , Glutamine/metabolism , Host-Parasite Interactions , Linolenic Acids/metabolism , Manduca/physiology , Oxylipins/metabolism , Plant Leaves/parasitology , Nicotiana/genetics , Nicotiana/parasitology , alpha-Linolenic Acid/metabolism
6.
New Phytol ; 190(3): 640-52, 2011 May.
Article in English | MEDLINE | ID: mdl-21284648

ABSTRACT

• Jasmonates are ubiquitous messengers in land plants essential for the activation of defense responses. However, their signaling properties, accumulation and metabolism vary substantially among species. Solanum nigrum is a wild Solanaceous species developed as a model to study defense responses. • Solanum nigrum plants transformed to silence the expression of key genes in jasmonate production (SnLOX3), conjugation (SnJAR4) and perception (SnCOI1) were generated to analyze the function of these genes in jasmonate accumulation and metabolism (studied by a combination of LC-MS/MS and (13) C-isotope labeling methods) and in signaling [studied by the systemic elicitation of leucine aminopeptidase (LAP) activity]. • In contrast with the early single jasmonic acid (JA) burst induced by wounding in wild-type (WT) plants, elicitation with insect oral secretions induced a later, second burst that was essential for the induction of systemic LAP activity, as demonstrated by ablation experiments. This induction was dependent on SnLOX3 and SnCOI1, but not on SnJAR4. In addition, the local accumulation of JA-glucose and JA-isoleucine was dependent on SnCOI1, whereas the accumulation of hydroxylated jasmonates was dependent on both SnCOI1 and SnJAR4. • The results demonstrate that SnLOX3, SnCOI1 and SnJAR4 have overlapping yet distinct roles in jasmonate signaling, differentially controlling jasmonate metabolism and the production of a systemic signal.


Subject(s)
Cyclopentanes/metabolism , Oxylipins/metabolism , Plant Proteins/metabolism , Signal Transduction , Solanum nigrum/metabolism , Animals , Cyclopentanes/chemistry , Gene Expression Regulation, Plant , Genes, Plant/genetics , Leucyl Aminopeptidase/metabolism , Manduca/physiology , Models, Biological , Oxylipins/chemistry , Plant Leaves/metabolism , Plants, Genetically Modified , RNA, Messenger/genetics , RNA, Messenger/metabolism , Solanum nigrum/enzymology , Solanum nigrum/genetics
7.
Plant Signal Behav ; 5(12): 1674-6, 2010 Dec.
Article in English | MEDLINE | ID: mdl-21150262

ABSTRACT

Plants can distinguish mechanical damage from larval folivory through the recognition of specific constituents of larval oral secretions (OS) which are deposited on the surface of leaf wounds during feeding. Fatty acid-amino acid conjugates (FACs) are major constituents of the OS of Lepidopteran larvae and they are strong elicitors of herbivore-induced defense responses in several plant species, including the wild tobacco Nicotiana attenuata. When OS from Manduca sexta larvae is deposited on N. attenuata wounded leaves, the major FAC N-linolenoyl-glutamic acid (18:3-Glu) is modified within seconds by a heat labile process. Some of the major modified forms are oxygenated products derived from 13-lipoxygenase activity and one of these derivatives, 13-oxo-13:2-Glu, is an active elicitor of enhanced JA biosynthesis and differential monoterpene emission in N. attenuata leaves.


Subject(s)
Insecta/physiology , Lipoxygenases/metabolism , Nicotiana/parasitology , Plant Leaves/parasitology , Animals
8.
BMC Plant Biol ; 10: 164, 2010 Aug 09.
Article in English | MEDLINE | ID: mdl-20696061

ABSTRACT

BACKGROUND: Some plants distinguish mechanical wounding from herbivore attack by recognizing specific constituents of larval oral secretions (OS) which are introduced into plant wounds during feeding. Fatty acid-amino acid conjugates (FACs) are major constituents of Manduca sexta OS and strong elicitors of herbivore-induced defense responses in Nicotiana attenuata plants. RESULTS: The metabolism of one of the major FACs in M. sexta OS, N-linolenoyl-glutamic acid (18:3-Glu), was analyzed on N. attenuata wounded leaf surfaces. Between 50 to 70% of the 18:3-Glu in the OS or of synthetic 18:3-Glu were metabolized within 30 seconds of application to leaf wounds. This heat-labile process did not result in free alpha-linolenic acid (18:3) and glutamate but in the biogenesis of metabolites both more and less polar than 18:3-Glu. Identification of the major modified forms of this FAC showed that they corresponded to 13-hydroxy-18:3-Glu, 13-hydroperoxy-18:3-Glu and 13-oxo-13:2-Glu. The formation of these metabolites occurred on the wounded leaf surface and it was dependent on lipoxygenase (LOX) activity; plants silenced in the expression of NaLOX2 and NaLOX3 genes showed more than 50% reduced rates of 18:3-Glu conversion and accumulated smaller amounts of the oxygenated derivatives compared to wild-type plants. Similar to 18:3-Glu, 13-oxo-13:2-Glu activated the enhanced accumulation of jasmonic acid (JA) in N. attenuata leaves whereas 13-hydroxy-18:3-Glu did not. Moreover, compared to 18:3-Glu elicitation, 13-oxo-13:2-Glu induced the differential emission of two monoterpene volatiles (beta-pinene and an unidentified monoterpene) in irlox2 plants. CONCLUSIONS: The metabolism of one of the major elicitors of herbivore-specific responses in N. attenuata plants, 18:3-Glu, results in the formation of oxidized forms of this FAC by a LOX-dependent mechanism. One of these derivatives, 13-oxo-13:2-Glu, is an active elicitor of JA biosynthesis and differential monoterpene emission.


Subject(s)
Glutamine/analogs & derivatives , Linolenic Acids/metabolism , Lipoxygenase/metabolism , Manduca/physiology , Nicotiana/enzymology , Plant Leaves/enzymology , Animals , Cyclopentanes/metabolism , Glutamine/metabolism , Lipoxygenase/genetics , Monoterpenes/analysis , Oxylipins/metabolism , Plant Leaves/chemistry , Nicotiana/genetics
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