JXB Advance Access originally published online on June 7, 2007
Journal of Experimental Botany 2007 58(10):2451-2462; doi:10.1093/jxb/erm111
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
© 2007 The Author(s).
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
This paper is available online free of all access charges (see http://jxb.oxfordjournals.org/open_access.html for further details)
RESEARCH PAPER |
A citrus abscission agent induces anoxia- and senescence-related gene expression in Arabidopsis
Horticultural Sciences Department, University of Florida, IFAS, Citrus Research and Education Center, 700 Experiment Station Road, Lake Alfred, FL 33850, USA
To whom correspondence should be addressed. E-mail: jkbu{at}ufl.edu
Received 11 December 2006; Revised 23 March 2007 Accepted 19 April 2007
 |
Abstract |
|---|
 Top Abstract IntroductionMaterials and methodsResultsDiscussionReferences |
|---|
The mechanisms of negative effects of 5-chloro-3-methyl-4-nitro-1H-pyrazole (CMNP), a pyrazole-derived plant growth regulator used as a citrus abscission agent, were explored in Arabidopsis by integrating transcriptomic, physiological, and ultrastructural analyses. CMNP promoted starch degradation and senescence-related symptoms, such as chloroplast membrane disruption, electrolyte leakage, and decreased chlorophyll and protein content. Symptoms of plant decline were evident 12 h after CMNP treatment. Microarray analysis revealed that CMNP influenced genes associated with stress, including those related to anoxia, senescence, and detoxification. Sucrose treatment arrested CMNP-induced plant decline. The results demonstrate that the plant response to CMNP shares common elements with various stresses and senescence at physiological and molecular levels.
Key words: Electrolyte leakage, microarray analysis, plant decline, stress
|
Introduction |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
The compound 5-chloro-3-methyl-4-nitro-1H-pyrazole (CMNP) is a plant growth regulator that advances abscission in mature Citrus sinensis fruit when applied to tree canopies and also plant decline in Arabidopsis thaliana when applied as a root drench (Alferez et al., 2005). CMNP acted as an uncoupler of energetic membranes, depleted total ATP content, and increased phospholipase A2 (PLA2) and lipoxygenase activities and production of downstream lipid signalling compounds. Moreover, CMNP reduced fruit detachment force, promoted starch breakdown and peel colour change by inducing total carotenoid accumulation and chlorophyll degradation, increased electrolyte leakage and membrane degradation, and induced protein catabolism in citrus fruit. In summary, CMNP promoted wounding-like symptoms in peel, accelerated senescence, and advanced abscission in citrus fruit (Alferez et al., 2006). Dinitrophenol also reduced mature fruit detachment force and accelerated abscission when applied to citrus canopies (Alferez et al., 2005). This implies that low molecular weight compounds with uncoupling activity may promote abscission.
Transcriptome-level analyses indicate that the plant response to various stresses involves changes in numerous metabolic and signal transduction pathways (Cheong et al., 2002; Kreps et al., 2002; Loreti et al., 2005). Application of plant growth regulators and other xenobiotic materials to plants alters gene expression associated with abiotic and biotic stresses and detoxification (Zhu and Wang, 2000; Ekman et al., 2003; Mezzari et al., 2005). Besides compound-specific responses, stress changes carbohydrate content and alters expression of genes involved in sugar metabolism (Provart et al., 2003). Under aerobic conditions, catabolism of carbohydrates involves metabolism of pyruvate by pyruvate dehydrogenase (PDH) and activation of cellular respiration. If oxidative phosphorylation is impaired by uncoupling or anoxic conditions, metabolism is switched to fermentation, and pyruvate is converted to acetaldehyde by pyruvate decarboxylase (PDC) and then to ethanol via alcohol dehydrogenase (ADH) (Smeekens, 2000). Under different biotic and abiotic stresses, including anoxia, hexokinases in general, and particularly fructokinases (FKs) and glucokinases, are activated, regulating sugar entry into glycolysis (Fox et al., 1998). In addition to anoxia-induced changes in carbohydrate metabolism, loss of complex carbohydrate and transient accumulation of soluble sugar is a feature of senescence (Buchanan-Wollaston et al., 2003).
Wounding alters local and systemic gene expression associated with carbohydrate metabolism at the wound site and throughout the plant (Delessert et al., 2004; Quilliam et al., 2006). Abscission occurs in young developing fruitlets if they unsuccessfully compete for carbohydrate (Gomez-Cadenas et al., 2000). Exogenous application of sugar stimulated the early phase and inhibited the late phase of senescence (Paul and Pellny, 2003), reduced fruitlet abscission (Iglesias et al., 2003), and enhanced tolerance to anoxia (Loreti et al., 2005). The role of sugar in reaction and recovery of plants to various stress conditions may be 2-fold: to provide carbon for reconstructive metabolism and to act as a signal eliciting downstream responses (Rolland et al., 2002).
In an attempt to understand further how responses to CMNP operate, some physiological- and transcriptional-level responses of Arabidopsis leaves to root application of CMNP were studied. Pyrazole, the parent compound of CMNP, is a constituent of some herbicides that are rapidly absorbed by roots of target plants and impact energetic machineries in plant cells (Duke et al., 2000). In addition to the uncoupling effect of CMNP, many substituted pyrazoles are also ADH inhibitors (Dahlbom et al., 1974). Inhibition of ADH by CMNP would reduce NAD-linked production of ATP in glycolysis and further reduce cellular energy supply, compromising cellular membrane integrity (Rawyler et al., 2002). We hypothesized that CMNP uncoupling action would modify expression of genes associated with carbon metabolism and energy supply, thus triggering plant response in Arabidopsis. The results demonstrate that genes associated with stress are influenced by root application of CMNP, and that providing a carbon source altered symptom development.
|
Materials and methods |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Plant material and treatments
Rossette leaves at positions 5 and 6 (stages 3.70–3.90, Boyes et al., 2001) from 4-week-old Arabidopsis thaliana adult plants were used. Seeds were stratified by imbibing at 4 °C for 48 h and then transferred to 4 cm deep trays containing potting medium (Metro Mix 500). Plants were grown in growth chambers for 2 weeks at 20 °C (10 h light at 300 µmol m–2 s–1 and 14 h dark) and then transferred to 26 °C under incandescent lamps (300 µmol m–2 s–1) with a 14 h light/10 h dark cycle for 1 week before treatment. Individual plants were removed from the tray and roots were immersed in beakers containing 50 ml of test solutions under continuous light (300 µmol m–2 s–1) at 26 °C. Leaves for soluble sugars, starch, total chlorophyll, and total protein analysis were harvested periodically up to 16 h after treatment. For electron microscopy, microarray, and real-time PCR analysis, samples taken at 0, 1, 3, and 6 h after treatment were used. Electrolyte leakage measurements were taken in leaves for periods up to 24 h after treatment. All test solutions contained Tween-20 (0.01%) as adjuvant.
Electron microscopy, electrolyte leakage, starch, and soluble sugar determination
For electron microscopy, mature leaves were excised from plants treated with 1.5 mM CMNP or water alone (control) and prepared as previously described (Burns et al., 1992). Soluble sugars and starch were quantified as described by Somogy (1952) with some modification. Arabidopsis leaves were dried at 60 °C for 3 d and ground to a powder. Samples (100 mg DW) were extracted with 80% ethanol and centrifuged twice for 1 min at 1000 rpm. To recover soluble sugars, HCl was added (1/100, v/v) to the supernatant and boiled for 10 min. For starch determination, pellets were treated overnight at 30 °C with a solution of 1 M MES (pH 5.0) and amyloglucosidase. Sample absorbance was measured at 520 nm in a spectrophotometer and compared with a standard curve of known glucose concentrations. Sugar and starch contents were calculated and expressed as a percentage of the control. Two biological replicates were used and sugar determinations were made in triplicate. Electrolyte leakage was determined in excised leaves immersed in 1.5 mM CMNP or water solutions, and measured as described (Alferez et al., 2006).
Chlorophyll and protein quantification
Leaves were collected for various times up to 12 h after treatment application. Chlorophyll was extracted with acetone and 0.1 g sodium carbonate at 4 °C for 1 d. Extract absorbance was measured at 645 nm and 663 nm, and chlorophyll content calculated using the Moran equation (Moran, 1982). Total protein content in extracts was measured by the dye binding method (Bio-Rad Laboratories, Hercules, CA, USA) using bovine serum albumin as standard (Bradford, 1976).
Microarray printing, probe labeling, hybridization, and data analysis
The Arabidopsis cDNA array was generated from the Arabidopsis Biological Resources Center's Arabidopsis bacterial clone set (www.tigr.org). Microarray slides were printed at the Keck Foundation Biotechnology Resource Laboratory, Yale University as described by Ma et al. (2001). Each slide contained two identical arrays, each containing 11 300 expressed sequence tags (ESTs; http://www.crec.ifas.ufl.edu/burns/PDF/supplement1.pdf) representing approximately 6000 unique genes.
Total RNA from samples treated with 1.5 mM CMNP or water was extracted from the leaves of 3-week-old Arabidopsis plants using phenol–chloroform. Total RNA was used as a template to synthesize Cy-3- or Cy-5-conjugated deoxy CTP-labelled cDNA probes with the CyScribe first strand cDNA labelling kit (Amersham Biosciences, USA) following the manufacturer's instructions. Three biological replicates provided three independent RNA extractions used for probe labelling, and three slides, each containing two duplicate arrays, were used for each comparison. One array on each slide was hybridized with one labelled sample pair; the remaining array was hybridized with the same sample pair labelled by swapped dyes. Slide pre-hybridization, probe hybridization, slide washing, and scanning were performed as described by Zhong and Burns (2003). Spot intensities were quantified with ScanAlyze software (Eisen et al., 1998; http://rana.lbl.gov/EisenSoftware.htm). Raw data generated by ScanAlyze were analysed by using a Visual Basic program called ArrayTeller (Zhong and Burns, 2003). The correlation coefficient of signals between different repetitions was calculated, and only replicates whose values were higher than 0.92 were considered for this study.
Sucrose effects on symptoms of CMNP-treated plants
For root dip treatments, the CMNP concentration of 1.5 mM was chosen based on progression of plant decline symptoms within a 12 h time span. Adult plants were treated with root dips of 1.5 mM CMNP, 1.5 mM CMNP+2% sucrose, 2% sucrose, or water alone for 12 h. After 12 h, plants were observed and symptoms documented.
Real-time PCR analysis of gene expression
Total RNA was prepared as described above, and contaminating DNA removed with RNase-free DNase (Qiagen). Quantitative PCR was performed with an ABI PRISM 7500 Sequence Detection System (Applied Biosystems) using the SYBR Green PCR kit (Applied Biosystems). Dilutions (10–1000-fold) of RNA were used in 25 µl reaction volumes to calculate the real-time efficiency of each sample. Relative expression ratios of target genes (GDH1, RCO, CHI, GLU, ADH1, PDC1, PDH, FK1, and TPS) were calculated in comparison with that of a constitutively expressed reference gene (ribosomal 18s) by the CT method using software from the ABI PRISM 7500 Sequence Detection System. To achieve comparable amplification of cDNA templates for r18s and target genes, RNA concentrations were diluted by 1/10 000 when amplified using r18s primers. Expression of r18s was normalized to a value of 1.0, and the relative expression of target genes was compared with the normalized value of r18s. The following specific primers were used: GDH1 (forward 5'-CAGGGCAGCGTTTTGTCAT-3' and reverse 5'-GCTTTGCCGCCCAAGAA-3'); RCO (forward 5'-CGACATTACTTCCATCACAAGCA-3' and reverse 5'-GGCCACACCTGCATGCA-3'); CHI (forward 5'-GCTTGTCCCGCAAATGGT-3' and reverse 5'-CGCCTCGTCGCTTGGA-3'); GLU (forward 5'-TGGGTGAGAGCAACATGCA-3' and reverse 5'-TGGCGTAGGTCAAGAGCAAGA-3'); ADH1 (forward 5'-GGAGGAGCAAGAGGGATAGGA-3' and reverse, 5'-ACTATCACATACGCGCCATTCTC-3'); PDC1 (forward 5'-AAGATTTCCAAACTCAGGCAAGAG-3' and reverse, 5'-ATGCAAGCCAAACAAAAACGA-3'); PDH (forward 5'- GGCGAGCACATTACCATCCT-3' and reverse, 5'- TTGCTGCCTGCATCACATG-3'), FK1 (forward 5'-GAGAGGCGCTTCTATTTGCAA-3' and reverse 5'-GGCATCGCCGGTATCG-3'); and TPS (forward 5'-TGGGATGAATCTTGTCAGTTATGAG-3' and reverse 5'-TGAGAATGAGGACGCCCTTT-3').
|
Results |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Physiological consequences of CMNP application
Transmission electron microscopy of CMNP-treated plants revealed that chloroplasts were visibly altered. In leaves of water-treated control plants, starch grains filled chloroplast stroma (Fig. 1A); these appeared similar to the CMNP treatment when observed 1 h after treatment (Fig. 1B). After 3 h, starch disappeared and plastoglobules were present (Fig. 1C). By 6 h after treatment, vesiculation and swelling were observed in thylakoid membranes, and the number of plastoglobules increased (Fig. 1D). Starch and soluble sugar content remained unchanged 1 h after CMNP treatment; however, after 3 h, starch declined and soluble sugars increased (Fig. 1E). Electrolyte leakage was unchanged until 3 h after CMNP application (Fig. 1F). By 24 h, a 60% increase in electrolyte leakage was measured in leaves treated with CMNP compared with the water-treated control. There was a marked loss of chlorophyll between 1 h and 2 h after CMNP application (Fig. 2A). Total leaf protein declined by 3 h after CMNP treatment and continued declining in a linear fashion, reaching 40% of the water-treated controls 12 h after treatment (Fig. 2B).
|
|
Transcriptional changes in response to CMNP
A summary of the functional distribution of genes up- and down-regulated by CMNP treatment is shown in Table 1, and Table 2 indicates expression of selected genes depicted in categories identified in Table 1 after 1, 3, and 6 h of CMNP treatment. These tables show genes up- or down-regulated by at least 2-fold. Genes associated with protein turnover/senescence, lipid signalling, detoxification, stress, and cell energetics/anoxia were up-regulated by CMNP treatment (Table 1). Several transcription/translation factors involved in regulation of various stresses and senescence responses were also induced. Increased treatment time increased expression of genes associated with detoxification and protein turnover/senescence. Transcripts down-regulated 1 h after CMNP application were associated with numerous metabolic areas. Increased treatment time increased the number of down-regulated genes related to sulphur metabolism and cellular structure. To confirm microarray results, nine marker genes for senescence, cell energetics, and stress were subjected to real-time PCR analysis (Table 3). Measured expression changes reflected changes determined in the arrays, demonstrating the fidelity of the microarray analysis.
|
|
|
Sucrose modified the response to CMNP
Control plants whose roots were treated with water showed no signs of wilting or stress (Fig. 3A, E). Visible leaf curl and dehydration occurred in plants exposed to CMNP (Fig. 3C, G). Addition of sucrose arrested this visible plant decline for 12 h (Fig. 3D, H); however, some wilting was observed after 24 h in the CMNP+sucrose treatment (data not shown). Sucrose alone promoted mild but transient leaf wilting 6 h after treatment (not shown), but plants appeared to recover after 12 h (Fig. 3B, F).
|
|
Discussion |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
This study integrates ultrastructural evidence with physiological and molecular data to examine the response of A. thaliana to CMNP, a pyrazole-derived plant growth regulator used as an abscission agent for citrus mature fruit. Some of the responses to CMNP in citrus advancing abscission, maturation, and senescence were similar to those caused by ethylene, although different mechanisms seemed to operate (Alferez et al., 2005). Previous work with the ethylene perception inhibitor 1-methylcyclopropene showed that ethylene perception was not required for effective fruit loosening in citrus after CMNP or ethephon treatments, or peel wounding (Kostenyuk and Burns, 2004; Pozo et al., 2004). These results raised the possibility of both ethylene-dependent and ethylene-independent physiological mechanisms leading to mature fruit abscission in citrus, and suggested that CMNP's mode of action was, at least in part, independent of ethylene.
Root application of CMNP promoted electrolyte leakage, disrupted thylakoid membranes, and altered carbohydrate metabolism in Arabidopsis leaves. Symptoms of plant decline followed. Microarray analysis indicated that CMNP impacted several areas of metabolism involved in stress signalling. In general, the biological response to CMNP shared elements common to anoxia responses (Gibbs and Greenway, 2003), wounding (Pohnert, 2002), acceleration of abscission (Roberts et al., 2002), and senescence (Buchanan-Wollaston et al., 2003).
Numerous transcription/translation factors induced in response to various regimes of oxygen deprivation in Arabidopsis were also identified in this study, including heat shock factors, AP2 domains, zinc fingers, and WRKY factors (Klok et al., 2002; Branco-Price et al., 2005; Liu et al., 2005; Loreti et al., 2005). In addition, genes involved in early responses to abiotic stress (drought and cold, DREB genes; salt, oxidative stress enzymes, and temperature, MYB transcription factors; Kreps et al., 2002; Xiong et al., 2002) appeared to be similarly involved in the response of Arabidopsis to CMNP. Furthermore, expression of genes associated with detoxification increased with time, indicating plant responses leading to inactivation of CMNP. Together, these results indicate that CMNP induced stress-related metabolism.
Previous work demonstrated that CMNP treatment reduced total cellular ATP content, increased oxygen uptake in isolated mitochondria, and collapsed the electrochemical gradient in isolated chloroplasts (Alferez et al., 2005). Anoxic stress gene expression was influenced by CMNP, supporting the conclusion that the compound causes uncoupling. One consequence of uncoupling would be loss of stored reserves (Rawyler et al., 2002). Starch reserves were depleted, and swelling of thylakoid membranes occurred with CMNP treatment. Although thylakoid swelling is a symptom of several stresses (Barcelo and Poschenrieder, 1990; Anttonen, 1992; Holopainen et al., 1992), it has also been observed in mutants of Chlamydomonas reinhardtii that lack ATP synthase (Majeran et al., 2001). Swelling of thylakoid membranes in chloroplasts of Arabidopsis by CMNP treatment may be a result of direct inhibition of ATPase activity or inhibition of ATP synthesis via collapse of the electrochemical gradient.
Activation of detoxification mechanisms was evident after CMNP treatment. Despite increased induction of such genes as treatment time increased, plants were not able to overcome the toxic effects of CMNP. By 6 h, wilting was visible, starch content declined, and thylakoid membranes were disrupted. By contrast, in citrus fruit, stored reserves recover from canopy CMNP treatments, although fruit eventually abscise (Alferez et al., 2005, 2006). Continuous root uptake may explain the severity of the effect of CMNP in Arabidopsis as compared with citrus fruit where the compound is sprayed on the fruit surface, uptake is reduced, and/or rapid detoxification reactions inactivate CMNP.
CMNP treatment resulted in loss of starch in Arabidopsis. Carbohydrate shortage due to fruitlet-to-fruitlet competition and defoliation activates abscission in flowers and young fruitlets (Mehouachi et al., 1996). Loss of starch reserves and increased soluble sugars were features common to CMNP-treated mature citrus fruit (Alferez et al., 2006). Carbohydrate demand may activate carbohydrate metabolism to compensate for loss of reserves induced by CMNP treatment. Release of sugars and subsequent phosphorylation by hexokinases may also have a signalling function (Fox et al., 1998). Increased expression of FK1, PDC1, ADH1, and TPS genes following CMNP treatment suggests anoxic and/or sugar transcriptional regulation of downstream responses in both citrus and Arabidopsis, and support common effects in carbohydrate metabolism in both systems as a response to CMNP application.
In the presence of an uncoupler such as CMNP, electron transport from NADH to oxygen proceeds in a normal fashion, but ATP is not synthesized. Loss of respiratory control leads to increased oxygen consumption. In a situation of uncoupler-impaired respiration, pyruvate concentration increases and becomes available for fermentation (Tadege et al., 1999). Although pyruvate oxidation via the citric acid cycle will also occur, the lower Km of PDH for its substrate ensures that enough pyruvate will be available for alcoholic fermentation via PDC1. Increased PDC1 and ADH1 expression has been associated with anoxia (Dolferus et al., 2004). However, once the carbohydrate pool was depleted, PDC1 and ADH1 expression decreased and plant decline could not be prevented. On the other hand, FK1 expression increased as the carbohydrate pool depleted, probably due to increased respiration and general induction by anaerobic stress (Fox et al., 1998).
Anoxia triggers significant changes in gene expression, and exogenous sugar availability enhances tolerance to anoxia (Vartapetian and Jackson, 1997). Application of sucrose reduced CMNP-associated symptoms of plant decline and may have provided carbon substrate for carbohydrate metabolism in the absence of food reserves throughout the plant. Sucrose has been shown to allow extended accumulation of certain anoxia-induced transcripts such as PDC and ADH after stress (Loreti et al., 2005). After sucrose addition, plants remained healthy probably because continuous supply of sugar helped to overcome stress due to energy shortage.
Trehalose phosphate synthase (TPS) is an essential enzyme since disruption of AtTPS1 leads to an embryo-lethal phenotype in Arabidopsis. Evidence suggests that TPS is involved in regulation of sugar metabolism (Eastmond et al., 2003). Trehalose, whose first synthesis step is catalysed by TPS, may function as a stress metabolite (Goddijn et al., 1997; Eastmond et al., 2003). In the present study, TPS was induced by CMNP after starch disappeared in chloroplasts, strengthening the idea that CMNP disturbs sugar metabolism and supporting a role for trehalose as a storage metabolite and stress protectant.
Membrane breakdown in chloroplasts was indicated by disruption of thylakoids and increasing presence of plastoglobules with time after CMNP treatment (Fig. 1B, C). Plastoglobules have been associated with breakdown of photosynthetic membranes, chloroplast disorganization, protein degradation, and amino acid turnover during senescence (Guiamet et al., 1999). Furthermore, plastoglobules increase in number and size in senescing chloroplasts as thylakoid membranes degrade (Tuquet and Newman, 1980). Chlorophyll loss and protein degradation are also common features of senescence in green tissues (Buchanan-Wollaston et al., 2003). Catabolism of membrane lipids is accelerated during senescence, and free fatty acids are released. These membrane breakdown products can act as second messengers involved in signal transduction. Activation of the lipid signalling cascade after CMNP treatment was illustrated by visible disorganization of membrane structures in chloroplasts and up-regulation of genes coding for patatin-like proteins, PLA2, phospholipase D (PLD), and 12-oxo-phytodiene reductase (OPR) before visual symptoms of membrane degradation. Additional evidence of membrane breakdown was shown by increased electrolyte leakage.
Sulphur assimilation and metabolism is crucial for plant survival during stress (Rausch and Wachter, 2005). Important compounds involved in xenobiotic detoxification, protein synthesis, and defence contain sulphur. The fact that sulphur metabolism-related genes were down-regulated by CMNP 6 h after treatment suggests that impaired detoxification and defence mechanisms could lead to rapid plant decline.
In conclusion, microarray and physiological data combined with ultrastructural observations in Arabidopsis show that root exposure to CMNP triggered signal cascades common to anoxia and senescence. The biological response to CMNP was characteristic of stresses associated with anoxia (Gibbs and Greenway, 2003), wounding (Pohnert 2002), acceleration of abscission (Roberts et al., 2002), and senescence (Buchanan-Wollaston et al., 2003). Lack of energy supply is a contributor to the final collapse of the functional cells, resulting in plant decline. The evidence presented indicated that exogenous sucrose applications provided short-term carbon necessary to maintain the plant, but could not overcome continuous CMNP exposure.
|
Footnotes |
|---|
* Present address: Citrus Research Institute, Chinese Academy of Agricultural Sciences, Citrus Village 15, Xiema Township, Beibei District, Chongqing, 400712, PR China.
|
Abbreviations |
|---|
ADH, alcohol dehydrogenase; CHI, chitinase; CMNP, 5-chloro-3-methyl-4-nitro-1H-pyrazole; FK, fructokinase; GLU, β-1,3 glucanase; GDH, glutamate dehydrogenase; PLA2,, phospholipase A2; PDC, pyruvate decarboxylase; PDH, pyruvate dehydrogenase; RCO, Rubisco, small subunit; TPS, trehalose phosphate synthase.
|
References |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Aida M, Ishida T, Fukaki H, Fujisawa H, Tasaka M. Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant. The Plant Cell (1997) 9:841–857.
Alban C, Baldet P, Axiotis S, Douce R. Purification and characterization of 3-methylcrotonyl-coenzyme A carboxylase from higher plant mitochondria. Plant Physiology (1993) 102:957–965.[Abstract]
Alferez F, Pozo L, Burns JK. Physiological changes associated with senescence and abscission in mature citrus fruit induced by 5-chloro-3-methyl-4-nitro-1H-pyrazole and ethephon application. Physiologia Plantarum (2006) 127:66–73.[CrossRef]
Alferez F, Singh S, Umbach A, Hockema B, Burns JK. Citrus abscission and Arabidopsis plant decline in response to 5-chloro-3-methyl-4-nitro-1H-pyrazole are mediated by lipid signaling. Plant, Cell and Environment (2005) 28:1436–1449.[CrossRef]
Anttonen S. Changes in lipids of Pinus sylvestris needles exposed to industrial pollution. Annals of Botany (1992) 29:89–99.
Barcelo J, Poschenrieder C. Plant water relations as affected by heavy metal stress: a review. Journal of Plant Nutrition (1990) 13:1–37.[Web of Science]
Both M, Csukai M, Stumpf MPH, Spanu PD. Gene expression profiles of Blumeria graminis indicate dynamic changes to primary metabolism during development of an obligate biotrophic pathogen. The Plant Cell (2005) 17:2107–2122.
Boyes DC, Zayed AM, Ascenzi R, McCaskill AJ, Hoffman NE, Davis KR, Gorlach J. Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. The Plant Cell (2001) 13:1499–1510.
Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Analytical Chemistry (1976) 72:248–254.
Bradley D. Isolation and characterization of a gene encoding a carboxypeptidase Y-like protein from Arabidopsis thaliana. Plant Physiology (1992) 98:1526–1529.
Branco-Price C, Kawaguchi R, Ferriera R, Bailey-Serres J. Differential mRNA translation contributes to modulation of gene expression in response to hypoxia stress in seedlings of Arabidopsis thaliana. Annals of Botany (2005) 96:647–660.
Buchanan-Wollaston V, Earl S, Harrison E, Mathas E, Navabpour S, Page T, Pink D. The molecular analysis of leaf senescence—a genomics approach. Plant Biotechnology Journal (2003) 1:3–22.[CrossRef][Web of Science][Medline]
Burns JK, Achor DS, Echeverria E. Ultrastructural studies on the ontogeny of grapefruit juice vesicles. Citrus paradisi Macf. cv Star Ruby. International Journal of Plant Science (1992) 153:14–25.[CrossRef][Web of Science]
Cheong YH, Chang H-S, Gupta R, Wang X, Zhu T, Luan S. Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiology (2002) 129:661–667.
Dahlbom E, Tolf B, Äkeson Ä, Lunquist C, Theorell H. On the inhibitory power of some further pyrazole derivatives of horse liver alcohol dehydrogenase. Biochemical and Biophysical Research Communications (1974) 57:549–553.[CrossRef][Web of Science][Medline]
Delessert C, Wilson IW, Van Der Straeten D, Dennis ES, Dolferus R. Spatial and temporal analysis of the local response to wounding in Arabidopsis leaves. Plant Molecular Biology (2004) 55:165–181.[CrossRef][Web of Science][Medline]
Dodeman VL, Le Guilloux M, Ducreux G. Characterization of storage proteins in Daucus carota L.: two novel proteins display zygotic embryo specificity. Plant and Cell Physiology (1998) 39:49–56.
Dolferus R, Jan Klok E, Delessert C, Wilson S, Ismond KP, Good AG, Peacock J, Dennis ES. Enhancing the anaerobic response. Annals of Botany (2004) 91:111–117.[CrossRef]
Duke SO, Dayan FE, Rimando AM. Natural products and herbicide discovery. In: Herbicides and their mechanisms of action—Cobb AH, Kirkwood RC, eds. (2000) Sheffield: Academic Press. 105–133.
Eastmond PJ, Li Y, Graham IA. Is trehalose-6-phosphate a regulator of sugar metabolism in plants? Journal of Experimental Botany (2003) 54:533–537.
Eisen MB, Spellman PT, Brown PO, Bostein D. Cluster analysis and display of genome-wide expression patterns. Proceedings of the National Academy of Sciences, USA (1998) 95:14863–14868.
Ekman DR, Lorenz WW, Przybyla AE, Wolfe NL, Dean JFD. SAGE analysis of transcriptome responses in Arabidopsis roots exposed to 2,4,6-trinitrotoluene. Plant Physiology (2003) 133:1397–1406.
Fox TC, Green BJ, Kennedy RA, Rumpho ME. Changes in hexokinase activity in Echinochloa phyllopogon and Echinochloa crus-pavonis in response to abiotic stress. Plant Physiology (1998) 118:1403–1409.
Fu H, Doeling JH, Rubin DM, Vierstra RD. Structural and functional analysis of the six regulatory particle triple-A ATPase subunits from the Arabidopsis 26s proteasome. The Plant Journal (1999) 18:529–540.[CrossRef][Web of Science][Medline]
Gibbs J, Greenway H. Mechanisms of anoxia tolerance in plants. I. Growth, survival and anaerobic catabolism. Functional Plant Biology (2003) 30:1–47.[CrossRef][Web of Science]
Goddijn OJM, Verwoerd TC, Voogd E, Krutwagen RW, de Graaf PT, van Dun K, Poels J, Ponstein AS, Damm B, Pen J. Inhibition of trehalase activity enhances trehalose accumulation in transgenic plants. Plant Physiology (1997) 113:181–190.[Abstract]
Gomez-Cadenas A, Mehouachi J, Tadeo FR, Primo-Millo E, Talon M. Hormonal regulation of fruitlet abscission induced by carbohydrate shortage in citrus. Planta (2000) 210:636–643.[CrossRef][Web of Science][Medline]
Goujon T, Minic Z, El Amrani A, Lerouxel O, Aletti E, Lapierre C, Joseleau J-P, Jouanin L. AtBXL1, a novel higher plant (Arabidopsis thaliana) putative beta-xylosidase gene, is involved in secondary cell wall metabolism and plant development. The Plant Journal (2002) 33:677–690.[CrossRef][Web of Science]
Guiamet JJ, Pichersky E, Nooden LD. Mass exodus from senescing soybean chloroplasts. Plant and Cell Physiology (1999) 40:986–992.
Guo Y, Cai Z, Gan S. Transcriptome of Arabidopsis leaf senescence. Plant, Cell and Environment (2004) 27:521–549.[CrossRef]
Gustavsson N, Kokke BPA, Harndahl U, Silow M, Bechtold U, Poghosyan Z, Murphy D, Boelens WC, Sundby C. A peptide methionine sulphoxide reductase highly expressed in photosynthetic tissue in Arabidopsis thaliana can protect the chaperone-like activity of a chloroplast-localized small heat shock protein. The Plant Journal (2002) 29:545–553.[CrossRef][Web of Science][Medline]
Hall JL. Cellular mechanisms for heavy metal detoxification and tolerance. Journal of Experimental Botany (2002) 53:1–11.
Hershko A, Ciechanover A, Heller H, Haas AL, Rose IA. Proposed role of ATP in protein breakdown: conjugation of proteins with multiple chains of the polypeptide of ATP-dependent proteolysis. Proceedings of the National Academy of Sciences, USA (1980) 77:1783–1786.
Hewezi T, Petitprez M, Gentzbittel L. Primary metabolic pathways and signal transduction in sunflower (Helianthus annuus L.): comparison of transcriptional profiling in leaves and immature embryos using cDNA microarrays. Planta (2006) 223:948–964.[CrossRef][Web of Science][Medline]
Holopainen T, Anttonen S, Wulff A, Palomaki V, Karenlampi L. Comparative evaluation of the effects of gaseous pollutants, acidic deposition and mineral deficiencies, structural changes in the cells of forest plants. Agriculture Ecosystems and Environment (1992) 42:365–398.[CrossRef]
Howarth JR, Dominguez-Solis JR, Gutierrez-Alcala G, Wray JL, Romero LC, Gotor C. The serine acetyltransferase gene family in Arabidopsis thaliana and the regulation of its expression by cadmium. Plant Molecular Biology (2003) 51:589–598.[CrossRef][Web of Science][Medline]
Hrabak EM, Chan CWM, Gribskov M, et al. The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiology (2003) 132:666–680.
Ibrahim AFM, Waters JA, Brown JWS. Differential expression of potato U1A spliceosomal protein genes: a rapid method for expression profiling of multigene families. Plant Molecular Biology (2001) 45:449–460.[CrossRef][Web of Science][Medline]
Iglesias DJ, Tadeo FR, Primo-Millo E, Talon M. Fruit set dependence on carbohydrate availability in citrus trees. Tree Physiology (2003) 23:199–204.
Izhaki A, Swain SM, Tseng T-S, Borochov A, Olszewski NE, Weiss D. The role of SPY and its TPR domain in the regulation of gibberellin action throughout the life cycle of Petunia hybrida plants. The Plant Journal (2001) 28:181–190.[CrossRef][Web of Science][Medline]
Joshi CP. Molecular biology of cellulose biosynthesis in plants. In: Recent research developments in plant molecular biology—Pandalai S, ed. (2003) Kerala, India: Research Signpost Press. 19–38.
Kieliszewski MJ, Lamport DT. Extensin: repetitive motifs, functional sites, post-translational codes, and phylogeny. The Plant Journal (1994) 5:157–172.[CrossRef][Web of Science][Medline]
Kim K-Y, Park S-W, Chung Y-S, Chung C-H, Kim J-I, Lee J-H. Molecular cloning of low-temperature-inducible ribosomal proteins from soybean. Journal of Experimental Botany (2004) 55:1153–1155.
Klok EJ, Wilson IW, Wilson D, Chapman SC, Ewing RM, Somerville SC, Peacock JW, Dolferus R, Dennis ES. Expression profile analysis of the low-oxygen response in Arabidopsis root cultures. The Plant Cell (2002) 14:2481–2494.
Koch JL, Nevins DJ. Tomato fruit cell wall. I. Use of purified tomato polygalacturonase and pectinmethylesterase to identify developmental changes in pectins. Plant Physiology (1989) 91:816–822.
Kostenyuk I, Burns JK. Mechanical wounding and abscission in citrus. Physiologia Plantarum (2004) 122:354–361.[CrossRef]
Kreps JA, Wu Y, Chang H-S, Zhu T, Wang X, Harper JF. Transcriptome changes for Arabidopsis in response to salt, osmotic and cold stress. Plant Physiology (2002) 130:2129–2141.
Kreuz K, Tommasini R, Martinoia E. Old enzymes for a new job. Herbicide detoxification in plants. Plant Physiology (1996) 111:349–353.[Web of Science][Medline]
Kwok SF, Staub JM, Deng X-W. Characterization of two subunits of Arabidopsis 19S proteasome regulatory complex and its possible interaction with the COP9 complex. Journal of Molecular Biology (1999) 285:85–95.[CrossRef][Web of Science][Medline]
Lam E, Lam YK-P. Binding site requirements and differential representation of TGA factors in nuclear ASF-1 activity. Nucleic Acid Research (1995) 23:3778–3785.
Lao NT, Schoneveld O, Mould RM, Hibberd JM, Gray JC, Kanavagh TA. An Arabidopsis gene encoding a chloroplast-targeted beta-amylase. The Plant Journal (1999) 20:519–527.[CrossRef][Web of Science][Medline]
Liu F, Vantoai T, Moy L, Bock G, Linford LD, Quackenbusch J. Global transcription profiling reveals novel insights into hypoxic response in Arabidopsis. Plant Physiology (2005) 137:1115–1129.
Lopukhina A, Dettenberg M, Weiler EW, Hollander-Czytko H. Cloning and characterization of a coronatine-regulated tyrosine aminotransferase from Arabidopsis. Plant Physiology (2001) 126:1678–1687.
Loreti E, Poggi A, Novi G, Alpi A, Perata P. A genome-wide analysis of the effects of sucrose on gene expression in Arabidopsis seedling under anoxia. Plant Physiology (2005) 137:1130–1138.
Ma H-M, Schulze S, Lee S, Yang M, Mirkov E, Irvine J, Moore P, Paterson A. An EST survey of the sugarcane transcriptome. Theoretical and Applied Genetics (2004) 108:851–863.[CrossRef][Web of Science][Medline]
Ma L, Li J, Qu L, Hager J, Chen Z, Zhao H, Deng XW. Light control of Arabidopsis development entails coordinated regulation of genome expression and cellular pathways. The Plant Cell (2001) 13:2589–2607.
Majeran W, Olive J, Drapier D, Vallon O, Wollman F-A. The light sensitivity of ATP synthase mutants of Chlamydomonas reinhardtii. Plant Physiology (2001) 126:421–433.
Martinez IM, Chrispeels MJ. Genomic analysis of the unfolded protein response in Arabidopsis shows its connection to important cellular processes. The Plant Cell (2003) 15:561–576.
Matvienko M, Wojtowicz A, Wrobel R, Jamison D, Goldwasser Y, Yoder JI. Quinone oxidoreductase message levels are differentially regulated in parasitic and non-parasitic plants exposed to allelopathic quinones. The Plant Journal (2001) 25:375–387.[CrossRef][Web of Science][Medline]
Mehouachi J, Serna D, Zaragoza S, Agusti M, Talon M, Primo-Millo E. Defoliation increases fruit abscission and reduces carbohydrate levels in developing fruits and woody tissues of Citrus unshiv. Plant Science (1995) 107:189–197.[CrossRef][Web of Science]
Mezzari MP, Walters K, Jelinkova M, Shih M-C, Just CL, Schnoor JL. Gene expression and microscopic analysis of Arabidopsis exposed to chloroacetanilide herbicides and explosive compounds. A phytoremediation approach. Plant Physiology (2005) 138:858–869.
Monroy AF, Sangwan V, Dhindsa RS. Low temperature signal transduction during cold acclimation: protein phosphatase 2A as an early target for cold-inactivation. The Plant Journal (1998) 13:653–660.[CrossRef][Web of Science]
Montiel G, Gantet P, Jay-Allemand C, Breton C. Transcription factor networks. Pathways to the knowledge of root development. Plant Physiology (2004) 136:3478–3485.
Moran R. Formulae for determination of chlorophyllous pigments extracted with N,N-dimethylformamide. Plant Physiology (1982) 69:1376–1381.
Motchoulski A, Liscum E. Arabidopsis NPH3: a NPH1 photoreceptor-interacting protein essential for phototropism. Science (1999) 286:961–964.
Munnik FW, Kerkmann K, Salamini F, Bartels D. Water deficit triggers phospholipase D activity in the resurrection plant Craterostigma plantagineum. The Plant Cell (2000) 12:111–124.
Mysore KS, Crasta OR, Tuori RP, Folkerts O, Swirsky PB, Martin GB. Comprehensive transcript profiling of Pto- and Prf-mediated host defense responses to infection by Pseudomonas syringae pv. Tomato. The Plant Journal (2002) 32:299–315.[CrossRef][Web of Science][Medline]
Neuteboom LW, Ng JMY, Kuyper M, Clijsdale OR, Hooykaas PJJ, van der Zaal EJ. Isolation and characterization of cDNA clones corresponding with mRNAs that accumulate during auxin-induced lateral root formation. Plant Molecular Biology (1999) 39:273–287.[CrossRef][Web of Science][Medline]
Pageau K, Reisdorf-Cren M, Morot-Gaudry J-F, Masclaux-Daubresse C. The two senescence-related markers, GS1 (cytosolic glutamine synthetase) and GDH (glutamate dehydrogenase), involved in nitrogen mobilization, are differentially regulated during pathogen attack and by stress hormones and reactive oxygen species in Nicotiana tabacum L. leaves. Journal of Experimental Botany (2006) 57:547–557.
Paul MJ, Pellny TK. Carbon metabolite feedback regulation of leaf photosynthesis and development. Journal of Experimental Botany (2003) 54:539–547.
Pohnert G. Phospholipase A2 activity triggers the wound-activated chemical defense in the diatom Thalassiosira rotula. Plant Physiology (2002) 129:1–9.
Porta H, Rocha-Sosa M. Plant lipoxygenases. Physiological and molecular features. Plant Physiology (2002) 130:15–21.
Pozo L, Yuan R, Kostenyuk I, Alferez F, Zhong G, Burns J. Combined applications of 1-methylcyclopropene and ethephon reduce defoliation but have no effects on mature fruit abscission in citrus. Journal of the American Society for Horticultural Science (2004) 129:473–478.
Provart NJ, Gil P, Chen W, Han B, Chang H-S, Wang X, Zhu T. Gene expression phenotypes of Arabidopsis associated with sensitivity to low temperatures. Plant Physiology (2003) 132:893–906.
Quilliam RS, Swarbrick PJ, Scholes JD, Rolfe SA. Imaging photosynthesis in wounded leaves of Arabidopsis thaliana. Journal of Experimental Botany (2006) 57:55–69.
Randall SK, Crowell DN. Protein isoprenylation in plants. Critical Reviews in Biochemistry and Molecular Biology (1999) 34:325–338.[CrossRef][Web of Science][Medline]
Rausch T, Wachter A. Sulfur metabolism: a versatile platform for launching defense operations. Trends in Plant Science (2005) 10:503–509.[CrossRef][Web of Science][Medline]
Rawyler A, Arpagaus S, Braendle R. Impact of oxygen stress and energy availability on membrane stability of plant cells. Annals of Botany (2002) 90:499–507.
Roberts JA, Elliott KA, Gonzalez-Carranza ZH. Abscission, dehiscence, and other cell separation processes. Annual Review of Plant Biology (2002) 53:131–158.[CrossRef][Medline]
Rolland F, Moore B, Sheen J. Sugar sensing and signaling in plants. The Plant Cell (2002) 14:S185–S205.
Salzman RA, Brady JA, Finlayson SA, et al. Transcriptional profiling of sorghum induced by methyl jasmonate, salicylic acid and aminocyclopropane carboxylic acid reveals cooperative regulation and novel gene responses. Plant Physiology (2005) 138:352–368.
Schaller F, Henning P, Weiler EW. 12-Oxophytodienoate-10,11-reductase: occurrence of two isozymes of different specificity against stereosiomers of 12-oxophytodienoic acid. Plant Physiology (1998) 118:1345–1351.
Schenk PM, Kazan K, Rusu AG, Manners JM, Maclean DJ. The SEN1 gene of Arabidopsis is regulated by signals that link plant defence responses and senescence. Plant Physiology and Biochemistry (2005) 43:997–1005.[CrossRef][Web of Science][Medline]
Schiffmann S, Schwenn JD. Isolation of cDNA clones encoding adenosine-5'-phosphosulfate kinase from Catharanthus roseus and an isoform (akn2) from Arabidopsis. Plant Physiology (1998) 117:1125.
Shi L, Gast RT, Gopalraj M, Olszewski NE. Characterization of a shoot-specific, GA3- and ABA-regulated gene from tomato. The Plant Journal (1992) 2:153–159.[Web of Science][Medline]
Shigeoka S, Ishikawa T, Tamoi M, Miyagawa Y, Takeda T, Yabuta Y, Yoshimura K. Regulation and function of ascorbate peroxidase isoenzymes. Journal of Experimental Botany (2002) 53:1305–1319.
Sicher RC, Hatch AL, Stumpf DK, Jensen RG. Ribulose 1,5-bisphosphate and activation of the carboxylase in the chloroplast. Plant Physiology (1981) 68:252–255.
Siminzsky B, Corbin FT, Ward ER, Fleischmann TM, Dewey RE. Expression of a soybean cytochrome P450 monooxygenase cDNA in yeast and tobacco enhances the metabolism of phenylurea herbicides. Proceedings of the National Academy of Sciences, USA (1999) 96:1750–1755.
Smalle J, Kurepa J, Haegman M, Gielen J, Van Montagu M, Van Der Straeten D. The trihelix DNA-binding motif in higher plants is not restricted to the transcription factors GT-1 and GT-2. Proceedings of the National Academy of Sciences, USA (1998) 95:3318–3322.
Smeekens S. Sugar-induced signal transduction in plants. Annual Review of Plant Physiology and Plant Molecular Biology (2000) 51:49–81.[CrossRef][Web of Science][Medline]
Smith AM, Zeeman SC, Smith SM. Starch degradation. Annual Review of Plant Biology (2005) 56:73–98.[CrossRef][Medline]
Somogy M. Notes on sugar determination. Journal of Biological Chemistry (1952) 195:19–23.
Sullivan TA, Jakobek JL, Lindgren PB. Cloning and characterization of a bean Udp-glucosyltransferase cDNA expressed during plant–bacterial interactions. Molecular Plant-Microbe Interactions (2001) 14:90–92.[CrossRef]
Tadege M, Dupuis I, Kuhlemeier C. Ethanolic fermentation: new functions for an old pathway. Trends in Plant Science (1999) 4:320–325.[CrossRef][Web of Science][Medline]
Taipalensuu J, Falk A, Rask L. A wound- and methyl jasmonate-inducible transcript coding for a myrosinase-associated protein with similarities to an early nodulin. Plant Physiology (1996) 110:483–491.[Abstract]
Toyama T, Teramoto H, Ishiguro S, Tanaka A, Okada K, Takeba G. A cytokinin-repressed gene in cucumber for a bHLH protein homologue is regulated by light. Plant and Cell Physiology (1999) 40:1087–1092.
Tuquet C, Newman DW. Aging and regreening in soybean cotyledons. 1. Ultrastructural changes in plastids and plastoglobuli. Cytobios (1980) 29:43–59.[Web of Science][Medline]
Uyemura SA, Luo S, Vieira M, Moreno S, Docampo R. Oxidative phosphorylation and rotenone-insensitive malate- and NADH-quinone oxidoreductases in Plasmodium yoelii mitochondria in situ. Journal of Biological Chemistry (2004) 279:385–393.
Van Parijs J, Broekaert WF, De Croylaan W, Peumans WJ. Hevein: an antifungal protein from rubber-tree (Hevea brasiliensis) latex. Planta (1991) 183:258–264.[Web of Science]
Vartapetian BB, Jackson MB. Plant adaptation to anaerobic stress. Annals of Botany (1997) 79:3–20.
Wang X. Plant phospholipases. Annual Review of Plant Physiology and Plant Molecular Biology (2001) 52:211–231.[CrossRef][Web of Science][Medline]
Weretilnyk EA, Alexander KJ, Drebenstedt M, Snider JD, Summesr P, Moffatt BA. Maintaining methylation activities during salt stress. The involvement of adenosine kinase. Plant Physiology (2001) 125:856–865.
Wu C-T, Bradford KJ. Class I chitinase and beta-1,3-glucanase are differentially regulated by wounding, methyl jasmonate, ethylene, and gibberellin in tomato seeds and leaves. Plant Physiology (2003) 133:263–273.
Wu C, Caspar T, Browse J, Lindquist S, Sommerville C. Characterization of an HSP70 cognate gene family in Arabidopsis. Plant Physiology (1988) 88:731–740.
Xiong L, Schumaker KS, Zhu J-K. Cell signaling during cold, drought and salt stress. The Plant Cell (2002) 14:S165–S183.
Yamasaki H, Sakihama Y, Ikehara N. Flavonoid-peroxidase reaction as a detoxification mechanism of plant cells against H2O2. Plant Physiology (1997) 115:1405–1412.[Abstract]
Zhao Y, Dai S, Blackwell EH, Schreiber SL, Chory J. SIR1, an upstream component in auxin signaling identified by chemical genetics. Science Express Report (2003) www.scienceexpress.org/31 july 2003/page1.
Zhong GY, Burns JK. Profiling ethylene-regulated gene expression in Arabidopsis thaliana by microarray analysis. Plant Molecular Biology (2003) 53:117–131.[CrossRef][Web of Science][Medline]
Zhu T, Wang X. Large-scale profiling of the Arabidopsis transcriptome. Plant Physiology (2000) 124:1472–1476.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  A. Malladi and J. K. Burns CsPLD{alpha}1 and CsPLD{gamma}1 are differentially induced during leaf and fruit abscission and diurnally regulated in Citrus sinensis J. Exp. Bot., October 1, 2008; 59(13): 3729 - 3739. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||