JXB Advance Access originally published online on September 24, 2004
Journal of Experimental Botany 2004 55(408):2533-2539; doi:10.1093/jxb/erh268
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RESEARCH PAPER |
Rubisco activase chaperone activity is regulated by a post-translational mechanism in maize leaves
1Departamento de Bioquímica y Biología Molecular de Plantas, Facultad de Química. Universidad Nacional Autónoma de México, 04510 México DF, Mexico
2Departamento de Biomedicina Molecular, Centro de Investigación y de Estudios Avanzados, Instituto Politécnico Nacional, 07300 México DF, Mexico.
To whom correspondence should be addressed. Fax: +52 5622 5329. E-mail: estelas{at}servidor.unam.mx
Received 8 March 2004; Accepted 22 July 2004
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Abstract |
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Rubisco activase (RCA) is a molecular chaperone present in maize as 43 kDa and 41 kDa polypeptides. They are encoded by two different genes comprising an identical ORF that corresponds to the 43 kDa RCA polypeptide, and their transcripts do not show putative splicing sites. To determine the origin of the 41 kDa polypeptide, leaf poly A+ mRNA was in vitro translated. Results demonstrated de novo synthesis only for the 43 kDa RCA. Antibodies developed against peptides from either the carboxy- or the amino-terminal end of 43 kDa RCA showed by western blot that the 43 kDa polypeptide amino-terminal region is missing in the 41 kDa polypeptide, whereas both RCA polypeptides shared the carboxy-end region. Regulation of RCA polypeptide ratios was determined in plant leaves at different developmental stages and under stressing environmental conditions. Increased levels of 43/41 kDa RCA ratio were found in leaves under low light exposure, whereas this ratio declined under water stress. Measurements of chaperone activity either on each RCA polypeptide alone or in a mixture showed the functional relevance of different 43/41 kDa RCA polypeptide ratios. Greater chaperone activity was found for the 41 kDa than for the 43 kDa polypeptide. Taken together, these results indicate that 41 kDa RCA polypeptide formation is regulated by limited proteolysis of the 43 kDa RCA at its amino-terminal region. This pathway is sensitive to developmental and environmental signals, and seems to play a relevant function during plant stress.
Key words: Developmental/environmental regulation, molecular chaperone, post-translational processing, Rubisco activase, Zea mays
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) is a widely distributed enzyme that catalyses the photosynthetic assimilation of atmospheric CO2 in chloroplasts of higher plants. Rubisco is a complex multisubunit enzyme regulated by different mechanisms. High rates of CO2 fixation by Rubisco are possible because of the action of Rubisco activase (RCA), a nuclear-encoded protein linked to a transit peptide sequence for its placement inside the chloroplast (Portis, 1990
). A variable number of rca genes have been reported in different plant species. In dicotyledonous plants, RCA is encoded by one (Werneke et al., 1988) to five genes (Qian and Rodermel, 1993), whereas in monocotyledonous plants, two genes have been detected (Rundle and Zielinski, 1991a; Ayala-Ochoa et al., 2004; Zhang and Komatsu, 2000). Two mature RCA polypeptides, with molecular mass ranging between 41 kDa and 47 kDa are present in most plants (Salvucci et al., 1987). In C3 plants, either a differential splicing at the intron nearest the 3' end of a pre-mRNA (Werneke et al., 1989; Rundle and Zielinski, 1991a; To et al., 1999) or the expression of two different genes without this regulation (Salvucci et al., 2003) can account for these polypeptides which differ in length at the carboxy-terminal region. The presence of the long carboxy terminus on the larger RCA polypeptide has been implicated in the regulation of the RCA activity by the chloroplast redox state as the underlying basis for light activation of Rubisco (Zhang and Portis, 1999; Zhang et al., 2002).
RCA is a molecular chaperone that activates Rubisco by restoring its active structure through an ATP hydrolysis-dependent process (Sánchez-de-Jiménez et al., 1995) releasing the RuBP inhibitor from the inactive Rubisco–RuBP complex (Salvucci and Ogren, 1996). A combination of computerized methods and multiple sequence protein alignment have further indicated that RCA belongs to the AAA+ protein family, a class of chaperone-like ATPases (Neuwald et al., 1999).
In maize, a C4 plant, two rca genes (Ayala-Ochoa et al., 2004) and two RCA polypeptides of 43 kDa and 41 kDa (Martínez-Barajas et al., 1997; Morales et al., 1999) have been reported. Interestingly, the two rca transcripts, each one expressed from its corresponding gene, contain an identical open reading frame (ORF), and do not show putative splicing sites at their 3' regions (Ayala-Ochoa et al., 2004). This ORF accounts for the 43 kDa mature RCA polypeptide which, based on sequence similarity, seems to correspond to the short RCA polypeptide reported for other species (Werneke et al., 1989; Rundle and Zielinski 1991a; To et al., 1999; Salvucci et al., 2003). Thus, the above information leaves uncertain the origin and functional importance of the maize 41 kDa RCA polypeptide, which remains as a challenging goal. Within this frame, the objective of the present research was to contribute to the understanding of the regulation of 43 and 41 kDa RCA polypeptide levels in maize and to determine the relevance of their ratio for RCA chaperone function, with particular interest in investigating the mechanism that originates the 41 kDa RCA polypeptide. These data indicate that the 41 kDa RCA most probably arises by post-translational processing of the 43 kDa polypeptide at its amino-terminal region, the 43/41 kDa RCA polypeptide ratio being developmentally and environmentally regulated. Furthermore, changes in this ratio resulted in variations of the RCA chaperone activity.
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Materials and methods |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Plant material and growth conditions
Maize (Zea mays L., var. Chalqueño) seedlings were grown in soil pots in a greenhouse. For developmental analysis, whole third leaves at stages four to seven of development (Loza-Tavera et al., 1990
) were sampled at midday. Sampling was taken from plants grown in ‘winter conditions’ (23 ±2 °C under a 12/12 h light/dark photoperiod and 200 µE m–2 s–1) and ‘summer conditions’ (25±2 °C under a 14/10 h light/dark photoperiod and 400 µE m–2 s–1). The onset of the light period was at 07.00 h and 06.00 h, respectively. For diurnal regulation studies, whole third leaves at stage four of summer-grown plants were collected at different times throughout a 24 h period: 04.00, 05.30, 07.00, 12.00, 17.00, and 22.00 h. For environmental factors analysis, 14 d after germination, well-watered and illuminated winter-grown plants either continued the above treatment (control) or were transferred to low light intensity conditions (3 µE m–2 s–1) or to a non-irrigation regimen. Whole third leaves at stages four, five, and six were sampled at midday from each group after 7 d treatment. At this time, the relative water content of leaves from non-irrigated plants was about 45%. In all cases, three samples of at least four leaves each were collected and immediately frozen at –70 °C.
Leaf protein extraction and western blot
One gram of leaf per sample was ground with a mortar and pestle with liquid N2 until pulverized and 2 ml of extraction buffer [0.1 M Tricine (pH 8.1), 10 mM MgCl2, 10 mM NaHCO3, 5 mM EDTA, 10 mM DTT, containing either 1.0 mM PMSF, 2 mM benzamidine, and 0.01 mM leupeptine or a commercially available protease inhibitor cocktail (Complete from Roche Applied Science)] were added immediately. The slurry was centrifuged for 10 min at 18 600 g at 4 °C in a Beckman GS-15R centrifuge. The supernatant was used to determine the amount of total protein (Bradford, 1976). The samples were resolved by SDS-PAGE and blotted onto polyvinylidene difluoride (PVDF) membranes. RCA polypeptides were analysed by immunoreaction with protein A-sepharose-purified antibodies developed against spinach RCA. Anti-rabbit IgG antibody coupled to horseradish peroxidase was used as the secondary antibody. The enhanced chemiluminescence (ECL) western-blotting detection kit (Amersham) was used to develop the reaction. Immunoreacting bands were detected with PhosphorImager (Bio-Rad) and densitometric analysis performed with Quantity One software.
Purification of RCA polypeptides
Pulverized leaf samples were homogenized with extraction buffer and centrifuged for 20 min at 20 000 g. Proteins from the supernatant were precipitated with ammonium sulphate at 35% saturation, and the precipitate was collected. The resulting pellet was dissolved in buffer A [20 mM Bis-Tris-Propane (BTP), pH 7.0; 1 mM ATP; 10 mM MgCl2] and precipitated with polyethylene glycol 8000 at 17% (w/v) final concentration. The precipitate was centrifuged, washed, and dissolved in buffer A. Proteins were clarified by centrifugation for 20 min at 20 000 g and further resolved by preparative gel electrophoresis on SDS-polyacrylamide gel (10%). The 43 kDa and 41 kDa RCA polypeptides were cut out and electroeluted with 25 mM TRIS, 192 mM glycine, and 0.1% (w/v) SDS. Removal of SDS from samples was done by electrodialysis. The proteins were then concentrated by Centricon-30 and washed with buffer containing 10 mM Tricine, 1 mM PMSF, 2 mM benzamidine, and 10 µM leupeptine, and quantified according to Bradford (1976).
Peptide synthesis
Multiple antigenic peptides (MAPs) were synthesized on a polylysine core resin (Tam, 1988) using Fmoc/tBu chemistry on a Synergy Model 432A (Applied Biosystems), according to the general procedures described by Merrifield and Stewart (1965). The following were the synthesized peptides: D-A-M-K-T-G-S-F-F-K and A-K-E-V-E-G-D-E-A-D, corresponding to the deduced carboxy- and amino-terminal sequences of maize RCA cDNA clones, respectively (Ayala-Ochoa et al., 1998). After the synthesis, protecting groups of both 
-amino and the side chains of amino acids were removed from the peptide using standard protocols. Peptide purity was checked by reverse-phase HPLC using a Delta Pak C18 column (Millipore Corporation, Bedford, MA; 3.9x150 mm).
Polyclonal antibody generation
Polyclonal antibodies against synthesized MAPs and purified spinach RCA were generated in male New Zealand rabbits according to standard protocols (Harlow and Lane, 1988). Antibodies were affinity purified with protein A-Sepharose and their specificity to the corresponding peptides and protein was determined by ELISA. Antibody titre was: 1:3200 for both the carboxy- and the amino-terminal peptide antibody and 1:8000 for the spinach RCA antibody.
In vitro translation and RCA immunoprecipitation
Poly (A)+ mRNA (5 µg) isolated by the PolyATtract mRNA isolation system IV (Promega) was in vitro translated in a wheat germ extract (WGE) (Promega) containing 5 µCi of [35S]-methionine and incubated for 60 min at 30 °C according to the manufacturer's instructions. After the samples were precleared with a preimmune rabbit serum, they were incubated with anti-Rubisco activase serum. Proteins were released from the immunocomplex with loading buffer (Anderson and Blobel, 1983) and resolved by SDS-PAGE. The immunoreacting RCA proteins were blotted onto a PVDF membrane and detected by PhosphorImager.
Chaperone activity assay
Chaperone activity was assayed on the basis of insulin reduction analysis, as described by Holmgren (1979). This assay measures the thioredoxin catalytic rate on insulin disulphide bridges reduction by dithiothreitol, as the turbidity formation from insulin- free B chain precipitation by spectrophotometry at 650 nm. Chaperone protective activity on insulin reduction delays the onset of precipitation. The reaction mixture contained: 0.13 mM insulin, 2 mM EDTA, 0.33 mM DTT, 4 µM thioredoxin, and 0.13 mM RCA. Positive (GroEL) and negative (BSA) controls of chaperone activity were set at 0.13 mM concentration. Changes in absorbance values at 650 nm were continuously recorded for 3.5 h. The enzymatic reduction of insulin by thioredoxin without protective protein and the corresponding non-enzymatic reduction by DTT without thioredoxin were also performed as controls.
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Results |
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The 43 kDa RCA polypeptide is post-translationally processed
In maize leaves, two rca mRNAs derived from separate genes containing the same ORF (43 kDa mature protein) are expressed (Ayala-Ochoa et al., 2004
). As a first approach to investigate the origin of the 41 kDa RCA polypeptide, an in vitro WGE translation system was set up. Poly A+ mRNA extracted from maize leaves, containing both the two mature RCA polypeptides (Fig. 4, lane 1) and the two rca mRNAs (Ayala-Ochoa et al., 2004), was translated in this system in the presence of [35S]-methionine as the labelled precursor. A control sample containing poly A+ mRNA from spinach leaves was also included. After 60 min of reaction the resultant proteins were immunoprecipitated with RCA antibody, the precipitate resolved by SDS-PAGE and analysed by a PhosphorImager apparatus. Results showed, in the control sample, two radiolabelled polypeptides of 49 kDa and 53 kDa (Fig. 1, left, lane 2), corresponding to the two spinach RCA polypeptide precursors of the mature polypeptides (42 kDa and 45 kDa) observed in the western blot (Fig. 1, right, lane 2). On the other hand, translation products from maize mRNA poly A+ showed only one radioactive polypeptide of 49 kDa (Fig. 1 left, lane 1), closely corresponding to the size of the 43 kDa precursor. These results indicate that the 43 kDa RCA polypeptide is the only de novo synthesized RCA polypeptide in maize leaves.
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The above data prompted the authors to look for evidence supporting a 43 kDa polypeptide post-translational process that accounted for the 41 kDa RCA formation. To this end, the following strategy was designed: ten amino acid peptides containing the deduced-amino acid sequence either of the 3' (D-A-M-K-T-G-S-F-F-K) or the 5' (A-K-E-V-E-G-D-E-A-D) end from maize rca cDNA (Ayala-Ochoa et al., 1998
) were synthesized. Polyclonal antibodies were raised against these synthetic peptides and used to test the two maize RCA polypeptides by western blot. Results showed that both 43 kDa and 41 kDa polypeptides were recognized by the carboxy-terminal peptide antibody, as well as by the polyclonal antibody raised against spinach RCA (Fig. 2, lanes 1 and 2). On the other hand, only the 43 kDa, but not the 41 kDa RCA polypeptide, cross-reacted with the N-terminal peptide antibody (Fig. 2, lane 3). This result indicates that the 41 and 43 kDa RCA polypeptides share most of their amino acid sequence but their amino-terminal end, most probably eliminated from the 43 kDa RCA by specific peptidase cleavage. From this information and the results from the in vitro RCA mRNA translation, it can be concluded that post-translational processing exerted on 43 kDa RCA polypeptide is responsible for the 41 kDa polypeptide origin in maize leaves.
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Accumulation of the two RCA polypeptides is developmentally and environmentally regulated
To find out the effect of internal and external factors on 43 kDa RCA polypeptide processing, particular physiological and environmental conditions were analysed on RCA polypeptide levels in maize plants at different developmental stages. Accumulation of RCA polypeptides on maize seedling development was compared in two different seasons: summer (14 h daylight) and winter (12 h daylight). Whole third leaves corresponding to developmental stages 4 to 7 were sampled at midday and RCA protein was analysed in leaf extracts by western blot. As shown in Fig. 3B and C, plants grown in winter showed a predominance of 43 kDa RCA accumulation at all developmental stages, whereas the opposite was observed for the summer-grown plants. On the other hand, development-associated changes were observed for the 41 kDa peptide, decreasing in the winter-grown plants (Fig. 3B). To ensure these changes were not due to an experimental artefact, these experiments were also performed by applying a different protease inhibitor mixture (see Materials and methods) to the system. These profiles imply an important shift of the 43/41 kDa polypeptide ratio depending on the development season, indicating that the 43/41 kDa RCA peptide ratio is regulated during development, and probably varies depending on the length of the light period, light intensity and quality, and temperature.
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A circadian pattern of rca mRNA accumulation has been reported for several plant species (Martino-Catt and Ort, 1992
; Pilgrim and McClung, 1993; To et al., 1999), thus measurements of 43 kDa and 41 kDa RCA polypeptide accumulation within a 12/12 h light/dark period were performed further. Total soluble protein from the third leaf of maize seedlings at stage four of development was analysed by SDS-PAGE and western blot. The 43/41 kDa RCA ratio remained approximately constant during the illuminated period (07.00–17.00 h), but changed through the dark period (22.00–04.00 h) (Fig. 4), mainly due to a reduction in the 41 kDa RCA level, indicating the uneven regulation of the two RCA polypeptide forms. To examine the effect of adverse environmental factors on RCA protein level during the winter season, low light supply and drought conditions were tested separately. Plants grown for 14 d under controlled conditions (12/12 h light/dark, 200 µE m–2 s–1, daily watering, 25 °C), were divided into three groups: one was maintained without change (control), while the other two were either transferred to low light supply (30 µE m–2 s–1) or deprived of irrigation. Third leaves at developmental stages four, five, and six of each group were sampled after 7 d of the indicated treatment. As shown in Fig. 5, a more dramatic effect was observed for low light supply, where the 43/41 kDa RCA ratio increased nearly 2-fold compared with the control value. Water restriction, on the other hand, caused the 43/41 kDa RCA ratio to decrease by up to half of the control levels, particularly in leaves from stages five and six. All of the above-described results were reproduced at least three times and clearly indicate that the accumulation of each RCA isoform is differentially regulated by developmental and environmental cues.
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RCA chaperone activity: effect of the 43/41 kDa polypeptide ratios
Finally, RCA chaperone activity was measured based on its ability to prevent insulin precipitation after reduction of its -S–S- bridges (Holmgren, 1979
). Indeed, when disulphide bonds linking A and B polypeptides from insulin are reduced by dithiothreitol, free B chain becomes insoluble and precipitates. Chaperone activity correlates with the delay of the onset of precipitation. To analyse the effect of 43/41 kDa RCA polypeptide ratio on RCA molecular chaperone activity, different ratios of purified 43/41 kDa polypeptides were analysed by this assay. The system, containing the same RCA total concentration made of either 41 kDa or 43 kDa RCA alone, or combinations of 2-fold 43 kDa over 41 kDa RCA or 41 kDa over 43 kDa RCA, was incubated with insulin in the presence of thioredoxin. The protector effect of RCA on the insulin S–S bridges reduction and its consequent delay on precipitation was determined as a function of time. GroEL and BSA were also assayed in this system as positive and negative chaperone controls, respectively. As illustrated in Fig. 6, the protective activity of the molecular chaperone GroEL was evident, since a delayed onset of insulin precipitation of 60 min was observed as compared with BSA, the negative control. On the other hand, 43 kDa RCA polypeptide alone exhibited moderate chaperone activity (10 min later than BSA), whereas the combination of both RCA polypeptides increased it, with the mixture containing the higher 41 kDa amount showing the better chaperone activity (40 min and 28 min, respectively, later than BSA) (Fig. 6). On the other hand, the 41 kDa RCA polypeptide caused the longest delay (135 min later than BSA), thus providing the highest protection to insulin precipitation, even greater than the positive control. These in vitro experimental results strongly suggest a biological significance for the 43/41 kDa RCA polypeptide ratios in maize.
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Discussion |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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An alternative splicing at the intron nearest the 3' end of an rca pre-mRNA (Werneke et al., 1989
; Rundle and Zielinski, 1991a; To et al., 1999) or the expression of separate genes (Salvucci et al., 2003) can account for the two RCA polypeptides observed in both dicot and monocot C3 plants. It is reported here that, in maize, a C4 plant, expression of the small 41 kDa RCA polypeptide does not arise by the same mechanism; rather, these data support the interpretation of post-translational processing at the amino-terminal region of the 43 kDa polypeptide as the most likely mechanism to generate the 41 kDa RCA form. Indeed, the in vitro translation experiment, where poly A+ mRNA from leaves that contained both RCA polypeptides and the two rca transcripts, showed de novo synthesis of only one RCA polypeptide (Fig. 1), and strongly supports this interpretation. Furthermore, this mechanism is consistent with the fact that the two maize RCA polypeptides cross-reacted with a carboxy-terminal specific antibody, but only the large one recognized the amino-terminal antibody (Fig. 2). Thus, the post-translational processing mechanism provides an explanation for the apparent paradox of two rca mRNAs in maize that contain the same and only ORF, but lack canonical consensus signals for RNA alternative splicing at their 3' and 5' ends (Ayala-Ochoa et al., 2004) and the presence of two RCA polypeptides in maize leaves. In agreement, expression of other proteins developmentally regulated by limited proteolysis processing has also been reported in plants (Pipal et al., 2003).
In general terms, molecular chaperones act as large complexes made of different polypeptides subunits (Sigler et al., 1998). In agreement with these data, variations in RCA chaperone activity were associated with the 43 kDa/41 kDa RCA polypeptide ratio (Fig. 6). Furthermore, the RCA ATP hydrolysis activity dependence on the aggregation state of its monomers (Lilley and Portis, 1997) is consistent with the above data. Actually, the larger oligomeric structures of RCA exhibited the maximal ATP hydrolysis and Rubisco activation activities (Wang et al., 1993). Therefore, regulation of the RCA subunit content and composition, particularly under adverse environmental conditions, would provide better protection for metabolic cell performance.
Differential accumulation of the two RCA polypeptides in maize during leaf development (Fig. 3), or environmental changes such as: day/night cycle (Fig. 4), low light intensity (Fig. 5), and water-stress (Fig. 5), also occur in other plants (Rundle and Zielinski, 1991b; Sánchez-de-Jiménez et al., 1995; Law et al., 2001; Rokka et al., 2001; Crafts-Brandner and Salvucci, 2002; Salekdeh et al., 2002), and are in accordance with the RCA molecular chaperone role. Thus, although the in vivo RCA subunit heteroligomerization and its relevance have not been unravelled (Salvucci and Ogren, 1996; Portis, 2003), the specific 43/41 kDa polypeptide ratios associated with particular physiological situations (Figs 1–3
) as well as the differences of in vitro chaperone activities (Fig. 6), strongly support the functional biochemical significance for in vivo RCA subunits ratio.
Chaperones contribute to fold a wide range of structurally and functionally unrelated proteins (Wang et al., 2002). As a chaperone, it is possible that RCA might also act on molecules other than Rubisco. Accordingly, it has been proposed that upon heat-shock, RCA would protect the thylakoid-associated protein synthesis machinery against heat inactivation (Rokka et al., 2001). It was also found that the RCA protein is expressed in monocot and dicot seeds (data not shown), where the Rubisco holoenzyme does not occur, further supporting an alternative function of the RCA chaperone.
In summary, a novel mechanism that accounts for the regulation of the RCA polypeptide content in maize leaves is reported here. It consists of 43 kDa RCA polypeptide synthesis and regulated specific proteolysis at its amino-terminal region for 41 kDa RCA polypeptide formation. This mechanism is dependent on developmental and environmental signals and results in variations of the RCA chaperone activity. Identification of the endopeptidase responsible for the processing of the 43 kDa RCA polypeptide will provide further insight into the functional regulation of RCA activity in maize.
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Acknowledgements |
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We are grateful to Dr Herminia Loza-Tavera for critical and helpful discussions. This work was partially supported by the doctoral CONACYT fellowships to MVS and AAO.
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Footnotes |
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* In memory of Alfredo Ayala-Ochoa.
Present address: Dirección de Investigación en Inmunotecnología, Laboratorios Silanes SA de CV Amores, 1304 Colonia del Valle, 03100 México DF, México.
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 A. P. Giri, H. Wunsche, S. Mitra, J. A. Zavala, A. Muck, A. Svatos, and I. T. Baldwin Molecular Interactions between the Specialist Herbivore Manduca sexta (Lepidoptera, Sphingidae) and Its Natural Host Nicotiana attenuata. VII. Changes in the Plant's Proteome Plant Physiology, December 1, 2006; 142(4): 1621 - 1641. [Abstract] [Full Text] [PDF]
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