JXB Advance Access originally published online on February 22, 2006
Journal of Experimental Botany 2006 57(4):767-774; doi:10.1093/jxb/erj087
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
FOCUS PAPER |
Phloem sap proteins: their identities and potential roles in the interaction between plants and phloem-feeding insects
Max Planck Institute of Molecular Plant Physiology, Department Willmitzer, Am Mühlenberg 1, D-14424 Potsdam, Germany
* To whom correspondence should be addressed. E-mail: kehr{at}mpimp-golm.mpg.de
Received 11 July 2005; Accepted 6 December 2005
 |
Abstract |
|---|
Top
Abstract
IntroductionThe phloem is a well-known target of sucking and piercing insects that utilize the transported fluid as their major nutrient source. In addition to small molecules like sugars and amino acids, phloem sap of higher land plants contains proteins that can accumulate up to high concentrations. Although the knowledge about the identities of these phloem sap proteins is increasing, the functions of most of them are still poorly understood. Since many phloem sap proteins have predicted roles in wound and defence responses, they constitute a class of compounds that can potentially influence plant–insect interactions. However, there are as yet no studies published that have examined direct effects of phloem sap proteins on insect feeding or vice versa. This review summarizes the current knowledge about the identities of phloem sap proteins, focused on polypeptides with probable functions in wound and defence reactions, and their potential impact on plant–insect interactions is discussed.
Key words: Phloem sap, plant–insect interactions, proteins
|
Introduction |
|---|
The phloem is the major route for the translocation and distribution of organic metabolites assimilated during photosynthesis. The sieve elements (SEs) transport a wide range of compounds like water, minerals, amino acids, organic acids, sugars, and sugar alcohols (Zimmermann and Ziegler, 1975
).
Research in recent years has shown that the phloem system is not only responsible for photosynthate allocation, but has several additional functions. For example, the phloem is an important mediator of whole-plant communication (Ruiz-Medrano et al., 2001). The transported information molecules include phytohormones (Baker, 2000), and also macromolecules such as proteins (Pearce, 1991) and RNAs (Jorgensen et al., 1998; Jorgensen, 2002). The occurrence of macromolecules seems surprising, since mature SEs lack the capability for mRNA and protein synthesis. However, recent studies have provided accumulating evidence that these macromolecules only not sporadically appear, but a large number of RNAs (Lucas et al., 2001) and soluble proteins (Hayashi et al., 2000; Walz et al., 2004) are constantly present in SE exudate. Proteins can even be regarded as a major component of phloem sap, given that, for example, cucurbit exudate contains high concentrations up to 100 mg ml–1 (Richardson et al., 1982). Phloem sap proteins are believed to be imported through specialized plasmodesmata connecting SEs and the adjacent companion cells (CCs) where protein synthesis is taking place (Smith et al., 1987; Clark et al., 1997; Dannenhoffer et al., 1997).
An increasing number of phloem sap polypeptides have been identified in recent years. However, identification and analysis of phloem sap proteins is hampered by the inaccessibility of the phloem stream to sampling attempts, and there are only a few plant species from which SE exudate can easily be obtained in sufficient quantities to analyse the proteins. Due to these sampling difficulties, most SE proteins identified originate from Ricinus, cucurbits, and oilseed rape, where relatively large amounts of phloem sap simply exude from incisions (Milburn, 1970). A few abundant proteins have also been specified in rice, where phloem-feeding insects allow the collection of small amounts of phloem sap (Kennedy and Mittler, 1953; Kawabe et al., 1980). Table 1 lists all known phloem sap proteins that have predicted functions in signalling, stress or defence reactions.
|
Interestingly, most of the identified phloem sap proteins repeatedly occur in more than one plant species (Table 1). This indicates a high degree of conservation of the phloem sap protein composition in higher land plants. A similar conclusion can be drawn from immunological studies (Schobert et al., 1998
) that showed that several proteins were found in the phloem sap of many, even completely unrelated, monocot and dicot species. Since current knowledge about phloem sap proteins is far from being complete in all species, it can be expected that even more proteins coincide in several plants, although some species-specific differences might exist. This reasonable degree of conserved proteins can be explained by the pronounced structural similarity of SEs in all angiosperms (van Bel, 1999) that is probably caused by the high functional specialization of SEs. |
Potential influences of phloem sap proteins on plant–insect interactions |
|---|
The transported metabolites make SEs an attractive target for insects that are specialized to feed exclusively on phloem sap, like, for example, whiteflies or aphids.
In contrast to herbivores, phloem-feeding insects establish a sustained interaction with SEs. They release saliva that inhibits plant stress responses and prevents closure of pierced SEs by callose or polymerized proteins (Miles, 1999). This allows the insects to ingest large amounts of phloem sap to obtain enough nutrients for their survival. Due to this feeding behaviour, phloem-sucking insects are directly exposed not only to nutrients but to all components of the transport fluid, including proteins. Interestingly, a high proportion of the phloem sap proteins so far identified is predicted to be involved in stress and defence reactions, although their exact physiological functions remain to be established. To date, there is no study showing either an impact of phloem sap proteins on insects or of insect feeding on phloem sap protein composition or activities. However, due to the direct contact of phloem-feeding insects to SE contents, an influence of phloem sap proteins on insects is easily conceivable.
At the whole plant level, phloem-feeding insects induce local responses, including the activation of salicylic- and jasmonic acid-dependent pathways (Moran and Thompson, 2001), although they cause only limited tissue damage to the plant when targeting SEs. In addition, genes involved in oxidative stress, calcium-dependent signalling, and pathogenesis-related responses [such as lipoxygenase, chitinases, peroxidases and other pathogenesis-related (PR) proteins] are key components of the plant defence response (Moran et al., 2002).
In addition to these local reactions, a recent publication demonstrated a systemic effect of aphid infestation on gene expression in isolated phloem tissue (containing sieve elements, companion cells, sclerenchyma, and parenchyma cells) of celery (Divol et al., 2005). Here, genes typically responding to non-chewing insects were not altered. Instead, genes involved in cell wall modification, water transport, vitamin biosynthesis, photosynthesis, and carbon and nitrogen assimilation were induced. This indicates that the phloem response might be quite different from the whole plant reaction.
However, the observed changes in phloem tissue gene expression do not allow conclusions about alterations of phloem sap protein composition, because the location of protein synthesis in CCs might differ from their site of accumulation in SEs.
The following sections will therefore focus on the known classes of defence-related phloem sap proteins summarized in Table 1 and will discuss how they could influence plant–insect interactions.
|
ROS, calcium and phytohormones |
|---|
As mentioned above, oxidative stress is one of the first general reactions to the injury caused by phloem-sucking insects penetrating the tissue. In addition, it has previously been noticed that aphid salivary secretions can themselves alter plant oxidative conditions (Jiang and Miles, 1993
; Walling, 2000). It was also proposed that the saliva and the injury caused by aphid feeding induce not only a local but also a systemic production of reactive oxygen species (ROS) in the phloem (Moran et al., 2002; Zhu-Salzman et al., 2004; Divol et al., 2005). Accordingly, several genes associated with oxidative stress are up-regulated by aphid infestation at the whole plant level in A. thaliana (Moran et al., 2002), as well as systemically in phloem tissue isolated from celery (Divol et al., 2005). In soybean, insect feeding has also been shown to trigger the generation of ROS. Here, a direct anti-insect activity of ROS has been proposed (Bi and Felton, 1995). ROS are obviously not excluded from SEs, since ROS scavenging enzymes are a protein class generally contained in phloem sap and their activities are up-regulated by stresses such as drought (Walz et al., 2002). Glutathione-S-transferases and the metal ion scavengers, metallothioneins, and the copper homeostasis factor can detoxify radicals (Marrs, 1996) and the expression of the corresponding genes was significantly up-regulated by aphid feeding in systemic phloem tissue (Divol et al., 2005). Phloem tissue-specific regulation of the redox status in response to insect attack is substantiated by the observation that even one week of aphid infestation of A. thaliana did not result in necrosis or other symptoms indicative of a breakdown in the regulation of oxidation (Moran et al., 2002).
In addition to ROS, tissue damage is normally accompanied by an elevation in cytosolic calcium. In undisturbed SEs, calcium is low and an increase upon wounding is thought to initiate a long-distance signalling cascade (Fromm and Bauer, 1994; Knoblauch et al., 2001; van Bel and Gaupels, 2004). It was proposed that elevations of phloem Ca2+ levels also participate in the regulation of phloem enzymes (Eschrich and Heyser, 1975). The occurrence of calcium-binding proteins in phloem sap was recognized early (McEuen et al., 1981), but some time elapsed before the first of them could be identified. For example, enzymes and activity of calcium-activated protein kinases that act as major mediators in Ca2+ signalling occur in phloem sap. In addition, annexins and calmodulins were found in phloem samples from different species (Table 1). There is evidence that calcium and calcium-binding proteins are involved in the regulation of plant wound responses (Bergey and Ryan, 1999; Leon et al., 2001) and reports actually suggest a relationship between calmodulin gene expression and ROS generation (Harding et al., 1997). Moreover, calmodulin expression is increased by systemin (Bergey and Ryan, 1999), a peptide hormone found in Solanaceae, that has also been detected inside SEs (Narvaez-Vasquez et al., 1995).
In addition, phloem sap contains enzymes involved in the synthesis of phytohormones, namely ethylene and the jasmonic acid (Table 1). Formation of these phytohormones within SEs may lead to an amplification of locally induced signals that can then trigger a systemic response, as has been proposed for jasmonic acid (Hause et al., 2003).
|
Occlusion of SEs |
|---|
It is well known that, upon mechanical damage, plants have different mechanisms to plug affected SEs to avoid the loss of organic nutrients. This can be regarded as a quick and straightforward response to the damage caused by insects. Calcium is an important mediator for plugging SEs and calcium antagonists such as EDTA have long been known to prevent this sieve tube occlusion (King and Zeevaart, 1974
).
Different mechanisms that are all based on the action of phloem sap proteins seem to be involved in SE occlusion responses. Legumes contain unique crystalloid proteins, the so-called forisomes, that can undergo rapid and reversible conversions from the condensed resting state into a dispersed state, in which they close SEs. Crystalloid dispersal is mediated by calcium levels that increase following plasma membrane leakage, rapid turgor loss, or mechanical injury (Knoblauch et al., 2001, 2003).
Another well-known class of SE proteins involved in the plugging of sieve pores are PP1 and PP2 that were first described in cucurbit phloem sap (Read and Northcote, 1983a), but seem to occur in all dicots. Under oxidative conditions, PP1 monomers and PP2 dimers are covalently cross-linked via disulphide bonds, forming high molecular weight polymers that close the sieve pores (Read and Northcote, 1983a, b). This response is normally accompanied by the synthesis of the ß-1,3-glucan callose by callose synthase that accumulates on sieve plates after different stress treatments (McNairn and Currier, 1968) to prevent assimilate loss from cut SEs (Sjölund, 1997). While the closure by proteins is a rapid and reversible mechanism, callose is responsible for long-term plugging of sieve plates that is almost irreversible (van Bel, 2003).
As a response to herbivore attack, phloem sap is squeezed from SEs and accumulates at wounded sites. This phloem sap will prevent further herbivory and reduces the risk of infection of wounds with opportunistic pathogens like fungi (Christeller et al., 1998). The formation of phloem filaments by PP1 and PP2 as well as the closure by callose constitute a potent physical barrier against further invasion.
By contrast, phloem-sucking insects can locate and access SEs avoiding the normal plant wound response. Components of aphid saliva injected immediately after phloem puncture inhibit the normal callose deposition and P-protein gelation and thus enable sap uptake without phloem sealing. After feeding sites are established, the stylets of phloem-piercing insects can stay in continuous contact with plant cells for h up to weeks (Walling, 2000). However, a recent study revealed that massive deposits of callose are caused by infestation with phloem-feeding aphids, with callose associated with sieve plates and the pore-plasmodesmata between CCs and their associated SEs. Even leaves that had been colonized by aphids, but from which the aphids were removed, showed extensive wound callose deposits, which persisted for up to 48 h after the removal of aphid colonies, suggesting that the damage caused by aphid feeding is a long-term, non-transient event in non-resistant plants (Botha and Matsiliza, 2004).
|
Anti-nutritive proteins |
|---|
If insects manage to overcome the first levels of plant defence, phloem sap still provides an option to inflict damage on them by supplying toxic or inhibitory compounds, including proteins. Plants can accumulate phloem sap proteins up to high concentrations. Since phloem sap accumulates at sites wounded by herbivores and also phloem-sucking insects take up large amounts of phloem sap, proteins with anti-insect properties constitute a passable route for directed plant defence responses. The first important question in this regard is if and how insects can take up and digest phloem sap proteins.
|
Uptake and digestion of phloem sap proteins by insects |
|---|
Insects with different feeding behaviours can be expected to get into contact with phloem sap by different mechanisms. Herbivores will undoubtedly ingest a portion of phloem sap together with the tissue consumed, while phloem-piercing insects can take up large quantities of phloem sap. Aphids normally process many times their body weight of phloem sap in order to assimilate sufficient quantities of amino acids, which occur in low concentrations in phloem, and defecate large amounts of sugars as honeydew, because the carbohydrate content of phloem exceeds their ability to use it (Law et al., 1992
). Therefore, toxic proteins transported in SEs could make sucking problematic for some phloem-feeding insects. Previous studies indicate that insects take up proteins from phloem sap together with all the other transport sap components without any obvious restrictions. Accordingly, phloem exudate collected from excised aphid stylets contains a range of different phloem proteins (Fisher et al., 1992; Ishiwatari et al., 1995; Barnes et al., 2004) and additional macromolecules like RNAs (Sasaki et al., 1998). Also the phloem-feeding whiteflies ingested leaf proteins from their diet when either a 35S-labelled mixture or a single fluorescently labelled protein was applied. 35S label was recovered either as labelled amino acids in honeydew or as labelled proteins and amino acids in the whiteflies' bodies (Salvucci et al., 1998). In a study of the aphid Acyrthosiphon pisum, proteins supplied with an artificial diet were recovered in intact form in honeydew (Rahbe et al., 1995), which provides direct evidence for protein ingestion by living aphids.
For insects feeding on plant tissues by chewing, proteolysis of dietary proteins is essential for survival. The widespread production of protease inhibitors (PIs) by plants in response to insect attack (Ryan, 1990) reflects the importance of this step.
However, in recent years the question whether piercing-sucking insects directly feeding on phloem sap are also dependent on protein digestion has been a matter of debate. Earlier studies suggested that phloem-sucking insects from the superorder Hemiptera do not contain significant levels of protease activity (Terra, 1990; Rahbe et al., 1995) and it was also shown that aphid salivary secretions contain no proteases (Cherqui and Tjallingii, 2000). Previously, the fact that lectins fed in artificial diets can be recovered intact in honeydew was interpreted as evidence against protein digestion (Rahbe et al., 1995). However, lectins are proteins that are very difficult to digest, even for herbivorous lepidopteran insects (Gatehouse et al., 1994). By contrast, more recent experiments indicate that the occurrence of proteases allowing digestive proteolysis might indeed be a more general feature, not only in herbivores but also in sap-sucking insects, and may be important for their proper nutrition (Salvucci et al., 1998; Foissac et al., 2002; Habibi et al., 2002; Cristofoletti et al., 2003).
|
Protease inhibitors and lectins |
|---|
One class of well-known defence proteins, the already-mentioned protease inhibitors, are widespread in phloem sap of different plant species (Table 1). Squash phloem exudate has been shown to contain high amounts of trypsin, chymotrypsin, serine, and aspartic protease inhibitors and cysteine protease inhibitors have also been detected in rape and Ricinus phloem sap (Table 1). PIs are proteins that tightly bind proteolytic enzymes and thereby inhibit their activity. Herbivores ingesting a diet high in PIs are thought to experience metabolic deficiencies, including the lack of essential amino acids (Ryan, 1990
). There is no question that protease inhibitors from plants can inhibit the digestive proteases of herbivorous insects and that they may, in certain instances, suppress growth, development, and survival when they are fed to these insects (Murdock and Shade, 2002). This led to the introduction of genes encoding protease inhibitors into plants by transgenic approaches in order to increase resistance towards chewing insects (Hilder et al., 1987; Gatehouse et al., 1997). The widespread distribution of PIs in vulnerable tissue and their wound- and herbivore inducibility in diverse plant families, together with the results from transgenic plants, demonstrate the important role of PIs against herbivores (Constable, 1999). The high abundance of PIs in phloem sap in concert with the growing evidence that also phloem-feeders contain digestive proteases (see above) suggests an important defensive role of the broad range of phloem sap PIs against herbivores as well as phloem feeders.
In addition to PIs, another group of defence proteins show a widespread occurrence in phloem sap, the lectins (Table 1). Lectins are proteins that reversibly bind to specific mono- or oligosaccharides. Chitin-binding lectins from the Cucurbitaceae are a small group of lectins that were first identified in cucurbit phloem sap (Read and Northcote, 1983b). Arabidopsis also contains homologous phloem-expressed PP2-like lectins (Dinant et al., 2003). In addition to PP2-like proteins, the phloem sap of different plants contains additional lectins (Table 1). Many lectins are toxic to both insects and also vertebrates, although only a few are known to be herbivore- or wound-induced (Chrispeels and Raikhel, 1991). In insects, dietary lectins are thought to bind to insect midgut tissue and disrupt feeding and digestion and thus interfere with growth and development (Murdock and Shade, 2002). Feeding experiments showed lectin effects on chewing (Murdock et al., 1990) and sucking (Powell et al., 1993) insects.
The anti-insect properties of lectins led to their biotechnological exploitation. The most intensely studied anti-insect lectin, snowdrop lectin (Galanthus nivalis agglutinin: GNA), showed a high toxicity against phloem-sucking insects, not only in tests with artificial diets but also in experiments with transgenic plants (Hilder et al., 1995; Down et al., 1996; Gatehouse et al., 1996), indicating that these toxins are translocated within the phloem sap. Accordingly, Shi et al. (1994) detected GNA lectin in the honeydew produced by aphids feeding on transgenic tobacco plants.
|
Other defence-related proteins |
|---|
Several components of the myrosinase system have been detected in phloem exudate from Brassica (Table 1). The myrosinase system is able to produce cyanates and nitriles (Bones and Rossiter, 1996
) from glucosinolates that are also transported inside the phloem (Chen et al., 2001). These toxic hydrolysis products are induced by wounding, micro-organisms, and insects and could lead to a deterrence of herbivorous as well as phloem-feeding insects.
Phloem sap contains additional proteins known to be induced by wounding (CSF-2, SN-1) or insect feeding (SLW-1, SLW-3), but whose modes of action are unknown. The SLW proteins are specifically induced by whitefly feeding. While SLW-1 transcription is regulated by jasmonic acid and ethylene, two phytohormones that can potentially be synthesized in SEs (see above), SLW-3 does not respond to any known wound signal, indicating a new signalling pathway for activation (Walling, 2000).
|
Conclusions |
|---|
The recent identification of a growing number of proteins from phloem sap of different plant species now allows first insights into the potential functions of these polypeptides. Functional classification maps them to diverse categories but, interestingly, a number of them are functionally related to defence responses and therefore influences on plant–insect interactions are conceivable.
The most likely functions are connected to instant wound signalling, plugging of SEs to avoid nutrient loss, and, since there is evidence that herbivores as well as phloem feeders are able to take up and digest phloem sap proteins, the dispersal of directly acting anti-insect polypeptides.
Future studies analysing the direct effects of insect infestation on local and systemic changes of phloem sap protein composition and activity will elucidate their exact involvement in plant defence against herbivores and phloem-sucking insects. This knowledge will be useful to develop novel biotechnological strategies to enhance the resistance of crop plants against phloem-feeding insects.
|
Footnotes |
|---|
Abbreviations: CC, companion cell; GNA, Galanthus nivalis agglutinin; PP1, phloem protein 1; PP2, phloem protein 2; PI, protease inhibitor; PR, pathogenesis-related; ROS, reactive oxygen species; SE, sieve element.
|
References |
|---|
Alosi MC, Melroy DL, Park RB. 1988. The regulation of gelation of phloem exudate from Cucurbita fruit by dilution, glutathione, and glutathione reductase. Plant Physiology 86, 1089–1094.
Avdiushko SA, Ye XS, Croft KP, Kuc J. 1997. Phosphorylation of proteins in cucumber exudates and evidence for protein kinase activity. Journal of Plant Physiology 150, 552–559.
Avdiushko SA, Ye XS, Kuc J, Hildebrand DF. 1994. Lipoxygenase is an abundant protein in cucumber exudates. Planta 193, 349–357.[Web of Science]
Baker DA. 2000. Vascular transport of auxins and cytokinins in Ricinus. Plant Growth Regulation 32, 157–160.
Barnes A, Bale J, Constantinidou C, Ashton P, Jones A, Pritchard J. 2004. Determining protein identity from sieve element sap in Ricinus communis L. by quadrupole time of flight (Q-TOF) mass spectrometry. Journal of Experimental Botany 55, 1473–1481.
Bergey D, Ryan C. 1999. Wound- and systemin-inducible calmodulin gene expression in tomato leaves. Plant Molecular Biology 40, 815–823.[CrossRef][Web of Science][Medline]
Bi JL, Felton GW. 1995. Foliar oxidative stress and herbivory: primary compounds, secondary metabolites, and reactive oxygen species as components of induced resistance. Journal of Chemical Ecology 21, 1511–1530.[CrossRef][Web of Science]
Bones AM, Rossiter JT. 1996. The myrosinase–glucosinolate system, its organization and biochemistry. Physiologia Plantarum 97, 194–208.[CrossRef]
Bostwick DE, Dannenhoffer JM, Skaggs MI, Lister RM, Larkins BA, Thompson GA. 1992. Pumpkin phloem lectin genes are specifically expressed in companion cells. The Plant Cell 4, 1539–1548.
Botha CEJ, Matsiliza B. 2004. Reduction in transport in wheat (Triticum aestivum) is caused by sustained phloem feeding by the Russian wheat aphid (Diuraphis noxia). South African Journal of Botany 70, 249–254.[Web of Science]
Chen S, Petersen BL, Olsen CE, Schulz A, Halkier BA. 2001. Long-distance phloem transport of glucosinolates in Arabidopsis. Plant Physiology 127, 194–201.
Cherqui A, Tjallingii WF. 2000. Salivary proteins of aphids, a pilot study on identification, separation and immunolocalization. Journal of Insect Physiology 46, 1177–1186.[CrossRef][Web of Science][Medline]
Chrispeels MJ, Raikhel NV. 1991. Lectins, lectin genes, and their role in plant defence. The Plant Cell 3, 1–9.[Medline]
Christeller JT, Farley PC, Ramsay RJ, Sullivan PA, Laing WA. 1998. Purification, characterization and cloning of an aspartic proteinase inhibitor from squash phloem exudate. European Journal of Biochemistry 254, 160–167.[Web of Science][Medline]
Clark AM, Jacobsen KR, Bostwick DE, Dannenhoffer JM, Skaggs MI, Thompson GA. 1997. Molecular characterization of a phloem-specific gene encoding the filament protein, Phloem Protein 1 (PP1), from Cucurbita maxima. The Plant Journal 12, 49–61.[CrossRef][Web of Science][Medline]
Constable CP. 1999. A survey of herbivore-inducible defensive proteins and phytochemicals. In: Agrawal AA, Tuzun S, Bent E, eds. Inducible plant defences against pathogens and herbivores: biochemistry, ecology, and agriculture. St Paul, MN, USA: American Phytopathological Society Press, 137–166.
Cristofoletti PT, Ribeiro AF, Deraison C, Rahbe Y, Terra WR. 2003. Midgut adaptation and digestive enzyme distribution in a phloem feeding insect, the pea aphid Acyrthosiphon pisum. Journal of Insect Physiology 49, 11–24.[CrossRef][Web of Science][Medline]
Dannenhoffer JM, Schulz A, Skaggs MI, Bostwick DE, Thompson GA. 1997. Expression of the phloem lectin is developmentally linked to vascular differentiation in cucurbits. Planta 201, 405–414.[CrossRef]
Dinant S, Clark AM, Zhu Y, Vilaine F, Palauqui J-C, Kusiak C, Thompson GA. 2003. Diversity of the superfamily of phloem lectins (phloem protein 2) in angiosperms. Plant Physiology 131, 114–128.
Divol F, Vilaine F, Thibivilliers S, Amselem J, Palauqui J-C, Kusiak C, Dinant S. 2005. Systemic response to aphid infestation by Myzus persicae in the phloem of Apium graveolens. Plant Molecular Biology 57, 517–540.[CrossRef][Web of Science][Medline]
Down RE, Gatehouse AMR, Hamilton WDO, Gatehouse JA. 1996. Snowdrop lectin inhibits development and decreases fecundity of the glasshouse potato aphid (Aulacorthum solani) when administered in vitro and via transgenic plants both in laboratory and glasshouse trials. Journal of Insect Physiology 42, 1035–1045.
Eschrich W, Heyser W. 1975. Biochemistry of phloem constituents. In: Zimmermann MH, Milburn JA, eds. Encyclopedia of Plant Physiology, Vol. 1. Berlin: Springer Verlag, 101–136.
Fisher DB, Wu Y, Ku MSB. 1992. Turnover of soluble proteins in the wheat sieve tube. Plant Physiology 100, 1433–1441.
Foissac X, Edwards MG, Du JP, Gatehouse AMR, Gatehouse JA. 2002. Putative protein digestion in a sap-sucking homopteran plant pest (rice brown plant hopper; Nilaparvata lugens: Delphacidae): identification of trypsin-like and cathepsin B-like proteases. Insect Biochemistry and Molecular Biology 32, 967–978.[CrossRef][Web of Science][Medline]
Fromm J, Bauer T. 1994. Action-potentials in maize sieve tubes change phloem translocation. Journal of Experimental Botany 45, 463–469.
Fukuda A, Okada Y, Suzui N, Fujiwara T, Yoneyama T, Hayashi H. 2004. Cloning and characterization of the gene for a phloem-specific glutathione S-transferase from rice leaves. Physiologia Plantarum 120, 595–602.[CrossRef][Medline]
Gatehouse AMR, Davidson GM, Newell CA, Merryweather A, Hamilton WDO, Burgess EJP, Gilbert RJC, Gatehouse JA. 1997. Transgenic potato plants with enhanced resistance to the tomato moth, Lacanobia oleracea: growth room trials. Molecular Breeding 3, 49–63.
Gatehouse AMR, Down RE, Powell KS, Sauvion N, Rabbe Y, Newell CA, Merryweather A, Hamilton WDO, Gatehouse JA. 1996. Transgenic potato plants with enhanced resistance to the peach-potato aphid Myzus persicae. Entomologia Experimentalis et Applicata 79, 295–307.
Gatehouse AMR, Powell KS, Peumans WJ, van Damme EJM, Gatehouse JA. 1994. Insecticidal properties of plant lectins: their potential in plant protection. In: Pusztai AJ, Bardocs S, eds. Lectins, biomedical perspectives. Basingstoke: Francis and Taylor, 35–57.
Giavalisco P, Kapitza K, Kolasa A, Buhtz A, Kehr J. 2006. Towards the proteome of Brassica napus phloem sap. Proteomics 6, 896–909.
Gomez G, Torres H, Pallas V. 2005. Identification of translocatable RNA-binding phloem proteins from melon, potential components of the long-distance RNA transport system. The Plant Journal 41, 107–116.[CrossRef][Web of Science][Medline]
Habibi J, Brandt SL, Coudron TA, Wagner RM, Wright MK, Backus EA, Huesing JE. 2002. Uptake, flow, and digestion of casein and green fluorescent protein in the digestive system of Lygus hesperus Knigh. Archives of Insect Biochemistry and Physiology 50, 62–74.[CrossRef][Web of Science][Medline]
Haebel S, Kehr J. 2001. Matrix-assisted laser desorption/ionization time of flight mass spectrometry peptide mass fingerprints and post source decay: a tool for the identification and analysis of phloem proteins from Cucurbita maxima Duch. separated by two-dimensional polyacrylamide gel electrophoresis. Planta 213, 586–593.[CrossRef][Web of Science][Medline]
Harding SA, Oh S-H, Roberts DM. 1997. Transgenic tobacco expressing a foreign calmodulin gene shows an enhanced production of active oxygen species. EMBO Journal 16, 1137–1144.[CrossRef][Web of Science][Medline]
Hause B, Hause G, Kutter C, Miersch O, Wasternack C. 2003. Enzymes of jasmonate biosynthesis occur in tomato sieve elements. Plant and Cell Physiology 44, 643–648.
Hayashi H, Fukuda A, Suzui N, Fujimaki S. 2000. Proteins in the sieve element–companion cell complexes: their detection, localization and possible functions. Australian Journal of Plant Physiology 27, 489–496.[Web of Science]
Hilder VA, Gatehouse AMR, Sheerman SS, Barker RS, Boulter D. 1987. A novel mechanism of insect resistance engineered into tobacco. Nature 330, 160–163.[CrossRef]
Hilder VA, Powell KS, Gatehouse AMR, et al. 1995. Expression of snowdrop lectin in transgenic tobacco plants results in added protection against aphids. Transgenic Research 4, 18–25.[CrossRef][Web of Science]
Ishiwatari Y, Honda C, Kawashima I, Nakamura S, Hirano H, Mori S, Fujiwara T, Hayashi H, Chino M. 1995. Thioredoxin h is one of the major proteins in rice phloem sap. Planta 195, 456–463.[Web of Science][Medline]
Jiang Y, Miles PW. 1993. Responses of a compatible lucerne variety to attack by spotted alfalfa aphid: changes in the redox balance in infested tissues. Entomologia Experimentalis et Applicata 67, 263–274.[CrossRef]
Jorgensen RA. 2002. RNA traffics information systemically in plants. Proceedings of the National Academy of Sciences, USA 99, 11561–11563.
Jorgensen RA, Atkinson RG, Forster RLS, Lucas WJ. 1998. An RNA-based information superhighway in plants. Science 279, 1486–1487.
Kawabe S, Bukomorita T, Chino M. 1980. Collection of rice phloem sap from stylets of homopterous insect severed by YAG laser. Plant and Cell Physiology 21, 1319–1327.
Kennedy J, Mittler T. 1953. A method of obtaining phloem sap via the mouth parts of aphids. Nature 171, 528.[Medline]
King R, Zeevaart J. 1974. Enhancement of phloem exudation from cut petioles by chelating agents. Plant Physiology 53, 96–103.
Knoblauch M, Noli GA, Müller T, Prüfer D, Schneider-Hüther I, Scharner D, van Bel AJE, Peters WS. 2003. ATP-independent contractile proteins from plants. Nature Materials 2, 600–603.[CrossRef][Web of Science][Medline]
Knoblauch M, Peters WS, Ehlers K, van Bel AJE. 2001. Reversible calcium-regulated stopcocks in legume sieve tubes. The Plant Cell 13, 1221–1230.
Krüger C, Berkowitz O, Stephan UW, Hell R. 2002. A metal-binding member of the late embryogenesis abundant protein family transports iron in the phloem of Ricinus communis L. Journal of Biological Chemistry 277, 25062–25069.
Law JH, Ribeiro JMC, Wells MA. 1992. Biochemical insights derived from insect diversity. Annual Review of Biochemistry 61, 87–111.[CrossRef][Web of Science][Medline]
Leon J, Rojo E, Sanchez-Serrano JJ. 2001. Wound signalling in plants. Journal of Experimental Botany 52, 1–9.
Lucas WJ, Yoo B-C, Kragler F. 2001. RNA as a long-distance information macromolecule in plants. Nature Reviews Molecular Cell Biology 2, 849–857.[CrossRef][Web of Science][Medline]
Marrs KA. 1996. The function and regulation of glutathione S-transferases in plants. Annual Review of Plant Physiology and Plant Molecular Biology 47, 127–158.[CrossRef][Web of Science][Medline]
McEuen AR, Hart JW, Sabnis DD. 1981. Calcium-binding protein in sieve tube exudate. Planta 151, 531–534.[CrossRef]
McNairn RB, Currier HB. 1968. Translocation blockage by sieve plate callose. Planta 82, 369–380.[CrossRef]
Milburn JA. 1970. Phloem exudation from castor bean: induction by massage. Planta 95, 272–276.[CrossRef]
Miles PW. 1999. Aphid saliva. Biological Reviews 74, 41–85.
Mira H, Martinez-Garcia F, Penarrubia L. 2001. Evidence for the plant-specific intercellular transport of the Arabidopsis copper chaperone CCH. The Plant Journal 25, 521–528.[CrossRef][Web of Science][Medline]
Moran PJ, Cheng Y, Cassell JL, Thompson GA. 2002. Gene expression profiling of Arabidopsis thaliana in compatible plant–aphid interactions. Archives of Insect Biochemistry and Physiology 51, 182–203.[CrossRef][Web of Science][Medline]
Moran PJ, Thompson GA. 2001. Molecular responses to aphid feeding in Arabidopsis in relation to plant defence pathways. Plant Physiology 125, 1074–1085.
Murdock LL, Huesing JE, Nielsen SS, Pratt RC, Shade RE. 1990. Biological effects of plant lectins on the cowpea weevil. Phytochemistry 29, 85–89.
Murdock LL, Shade RE. 2002. Lectins and protease inhibitors as plant defences against insects. Journal of Agricultural and Food Chemistry 50, 6605–6611.[CrossRef][Web of Science][Medline]
Murray C, Christeller JT. 1995. Purification of a trypsin inhibitor (PFTI) from pumpkin fruit phloem exudate and isolation of putative trypsin and chymotrypsin inhibitor cDNA clones. Biological Chemistry Hoppe-Seyler 376, 281–287.
Nakamura S, Hayashi H, Mori S, Chino M. 1993. Protein phosphorylation in the sieve tubes of rice plants. Plant and Cell Physiology 34, 927–933.
Narvaez-Vasquez J, Pearce G, Orozco-Cardenas ML, Franceschi VR, Ryan CA. 1995. Autoradiographic and biochemical evidence for the systemic translocation of systemin in tomato plants. Planta 195, 593–600.[Web of Science]
Pearce G. 1991. A polypeptide from tomato leaves induces wound-inducible proteinase inhibitor proteins. Science 253, 895–898.
Powell KS, Gatehouse AMR, Hilder VA, Gatehouse JA. 1993. Antimetabolic effects of plant lectins and plant and fungal enzymes on the nymphal stages of two important rice pests, Nilaparvata lugens and Nephotettix cinciteps. Entomologia Experimentalis et Applicata 66, 119–126.[CrossRef]
Rahbe Y, Sauvion N, Febvay G, Peumans WJ, Gatehouse AMR. 1995. Toxicity of lectins and processing of ingested proteins in the pea aphid Acyrthosiphon pisum. Entomologia Experimentalis et Applicata 76, 143–155.[CrossRef]
Read SM, Northcote DH. 1983a. Chemical and immunological similarities between the phloem proteins of three genera of the Cucurbitaceae. Planta 158, 119–127.[CrossRef]
Read SM, Northcote DH. 1983b. Subunit structure and interactions of the phloem proteins of Cucurbita maxima (pumpkin). European Journal of Biochemistry 134, 561–569.[Web of Science][Medline]
Richardson PT, Baker DA, Ho LC. 1982. The chemical composition of cucurbit vascular exudates. Journal of Experimental Botany 33, 1239–1247.
Ruiz-Medrano R, Xoconostle-Cazares B, Lucas WJ. 2001. The phloem as a conduit for inter-organ communication. Current Opinion in Plant Biology 4, 202–209.[CrossRef][Web of Science][Medline]
Ryan CA. 1990. Protease inhibitors in plants: genes for improving defences against insects and pathogens. Annual Review of Phytopathology 28, 425–449.[Web of Science]
Salvucci ME, Rosell RC, Brown JK. 1998. Uptake and metabolism of leaf proteins by the silverleaf whitefly. Archives of Insect Biochemistry and Physiology 39, 155–165.[CrossRef]
Sasaki T, Chino M, Hayashi H, Fujiwara T. 1998. Detection of several mRNA species in rice phloem sap. Plant and Cell Physiology 39, 895–897.
Schobert C, Baker L, Szederkenyi J, Großmann P, Komor E, Hayashi H. 1998. Identification of immunologically related proteins in sieve-tube exudate collected from monocotyledonous and dicotyledonous plants. Planta 206, 245–252.[CrossRef][Web of Science]
Shi Y, Wang MB, Powell KS, van Damme E, Hilder VA, Gatehouse AMR, Boulter D, Gatehouse JA. 1994. Use of rice sucrose synthase-1 promoter to direct phloem-specific expression of ß-glucuronidase and snowdrop lectin genes in transgenic tobacco plants. Journal of Experimental Botany 45, 623–631.
Sjölund RD. 1997. The phloem sieve element: a river runs through it. The Plant Cell 9, 1137–1146.[CrossRef][Web of Science][Medline]
Smith LM, Sabnis DD, Johnson RPC. 1987. Immunocytochemical localization of phloem lectin from Cucurbita maxima using peroxidase and colloidal-gold labels. Planta 170, 461–470.[CrossRef]
Szederkenyi J, Komor E, Schobert C. 1997. Cloning of the cDNA for glutaredoxin, an abundant sieve-tube exudate protein from Ricinus communis L. and characterization of the glutathione-dependent thiol-reduction system in sieve tubes. Planta 202, 349–356.[CrossRef][Web of Science][Medline]
Terra WR. 1990. Evolution of digestive systems of insects. Annual Review of Entomology 35, 181–200.[CrossRef][Web of Science]
van Bel AJE. 1999. Evolution, polymorphology and multifunctionality of the phloem system. Perspectives in Plant Ecology, Evolution and Systematics 2, 163–184.[CrossRef]
van Bel AJE. 2003. The phloem, a miracle of ingenuity. Plant, Cell and Environment 26, 125–149.[CrossRef]
van Bel AJE, Gaupels F. 2004. Pathogen-induced resistance and alarm signals in the phloem. Molecular Plant Pathology 5, 495–504.[CrossRef][Web of Science]
Walling LL. 2000. The myriad plant responses to herbivores. Journal of Plant Growth Regulation 19, 195–216.[Medline]
Walz C, Giavalisco P, Schad M, Juenger M, Klose J, Kehr J. 2004. Proteomics of curcurbit phloem exudate reveals a network of defence proteins. Phytochemistry 65, 1795–1804.[CrossRef][Web of Science][Medline]
Walz C, Juenger M, Schad M, Kehr J. 2002. Evidence for the presence and activity of a complete antioxidant defence system in mature sieve tubes. The Plant Journal 31, 189–197.[CrossRef][Web of Science][Medline]
Yoo B-C, Lee J-Y, Lucas WJ. 2002. Analysis of the complexity of protein kinases within the phloem sieve tube system. Characterization of Cucurbita maxima calmodulin-like domain protein kinase 1. Journal of Biological Chemistry 277, 15325–15332.
Yoo B-C, Aoki K, Xiang Y, Campbell LR, Hull RJ, Xoconostle-Cazares B, Monzer J, Lee J-Y, Ullman DE, Lucas WJ. 2000. Characterization of Cucurbita maxima phloem serpin-1 (CmPS-1). The Journal of Biological Chemistry 275, 35122–35128.
Zhu-Salzman K, Salzman RA, Ahn J-E, Koiwa H. 2004. Transcriptional regulation of Sorghum defence determinants against a phloem-feeding aphid. Plant Physiology 134, 420–431.
Zimmermann MH, Ziegler H. 1975. Transport in plants: phloem transport. In: Encyclopedia of plant physiology, Vol. 1. New York: Springer, 480–503.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  E Akman Gunduz and A.E Douglas Symbiotic bacteria enable insect to use a nutritionally inadequate diet Proc R Soc B, March 7, 2009; 276(1658): 987 - 991. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. Kutsukake, N. Nikoh, H. Shibao, C. Rispe, J.-C. Simon, and T. Fukatsu Evolution of Soldier-Specific Venomous Protease in Social Aphids Mol. Biol. Evol., December 1, 2008; 25(12): 2627 - 2641. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 F. Gaupels, A. Buhtz, T. Knauer, S. Deshmukh, F. Waller, A. J. E. van Bel, K.-H. Kogel, and J. Kehr Adaptation of aphid stylectomy for analyses of proteins and mRNAs in barley phloem sap J. Exp. Bot., September 1, 2008; 59(12): 3297 - 3306. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 K. Zhu-Salzman, D. S. Luthe, and G. W. Felton Arthropod-Inducible Proteins: Broad Spectrum Defenses against Multiple Herbivores Plant Physiology, March 1, 2008; 146(3): 852 - 858. [Full Text] [PDF]
|
|
|
|
|
|
C. Rispe, M. Kutsukake, V. Doublet, S. Hudaverdian, F. Legeai, J.-C. Simon, D. Tagu, and T. Fukatsu Large Gene Family Expansion and Variable Selective Pressures for Cathepsin B in Aphids Mol. Biol. Evol., January 1, 2008; 25(1): 5 - 17. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. A. Khan, Q. Wang, R. D. Sjolund, A. Schulz, and G. A. Thompson An Early Nodulin-Like Protein Accumulates in the Sieve Element Plasma Membrane of Arabidopsis Plant Physiology, April 1, 2007; 143(4): 1576 - 1589. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||