Journal of Experimental Botany, Vol. 53, No. 370, pp. 801-808,
April 15, 2002
© 2002 Oxford University Press
Original Papers |
What stay-green mutants tell us about nitrogen remobilization in leaf senescence
Institute of Grassland and Environmental Research, Plas Gogerddan, Aberystwyth, Ceredigion SY23 3EB, UK
Received 18 July 2001; Accepted 8 October 2001
 |
Abstract |
|---|
 Top Abstract IntroductionStay-green Festuca pratensisChlorophyll metabolism in stay...Genes expressed in stay-green...ConclusionReferences |
|---|
Leaf senescence has an important role in the plant's nitrogen economy. Chlorophyll catabolism is a visible symptom of protein mobilization. Genetic and environmental factors that interfere with yellowing tend to modify protein degradation as well. The chlorophyll–protein relationship is much closer for membrane proteins than it is for soluble or total leaf proteins. In stay-greens, genotypes with a specific defect in the chlorophyll catabolism pathway, soluble protein degradation during senescence may be close to normal, but light-harvesting and reaction centre thylakoid membrane proteins are much more stable. Genes for the chlorophyll catabolism pathway and its control are important in the regulation of protein mobilization. Genes for three steps in the pathway are reported to have been isolated. The gene responsible for the stay-green phenotype in grasses and legumes has not yet been cloned but a fair amount is known about it. Pigment metabolism in senescing leaves of the Festuca–Lolium stay-green mutant is clearly disturbed and is consistent with a blockage at the ring-opening (PaO) step in chlorophyll breakdown. PaO is de novo synthesized in senescence and thought to be the key enzyme in the chlorophyll a catabolic pathway. The stay-green mutation is likely to be located in the PaO gene, or a specific regulator of it. These genes may well be in the various senescence-enhanced cDNA collections that have been generated, but functional handles on them are currently lacking. When the stay-green locus from Festuca pratensis was introgressed into Lolium temulentum, a gene encoding F. pratensis UDPG-pyrophosphorylase was shown to have been transferred on the same chromosome segment. A strategy is described for cloning the stay-green gene, based on subtractive PCR-based analyses of intergeneric introgressions and map-based cloning.
Key words: Alien introgression, cDNA, chlorophyll catabolism, Festuca, Lolium, species-specific polymorphism, UDP-glucose pyrophosphorylase.
|
Introduction |
|---|
|
TopAbstractIntroductionStay-green Festuca pratensisChlorophyll metabolism in stay...Genes expressed in stay-green...ConclusionReferences |
|---|
Leaf senescence has an important role in the plant's nitrogen economy (Feller and Fischer, 1994
). When demand from sinks is not met by current assimilation, stored N is remobilized. Once low molecular weight reserves have been drained, polymers begin to be catabolized. Leaves, and particularly chloroplasts, are sites of protein accumulation. Mobilization of chloroplast protein is a central metabolic activity in leaf senescence. Ordinarily, when leaves senesce they turn yellow. Chlorophyll catabolism is a visible symptom of protein mobilization in leaf senescence. In general, yellowing and protein N remobilization are well correlated. This is illustrated by Fig. 1, in which the chlorophyll a+b content of Lolium temulentum leaf tissue measured at various times during senescence is plotted against total protein and shows a strong linear relationship (P<0.05). Genetic and environmental factors that interfere with yellowing tend to modify protein degradation as well. For example, a mutant gene that disables chlorophyll degradation was introgressed from Festuca pratensis into L. temulentum (Thomas et al., 1999). In this genotype, the broadly linear correlation between pigment and protein is still observed but the slope of the pigment–protein regression is markedly reduced (Fig. 1).
|
) and of a stay-green introgression line (•). The data comprise observations from four independent experiments and fitted regression lines and equations are shown.Most of the mobilizable protein in a leaf is soluble. Chlorophyll, on the other hand, is strictly confined to plastid membranes. The chlorophyll–protein relationship is much closer for membrane proteins than it is for soluble or total leaf proteins. If chlorophyll breakdown in senescence is prevented, soluble and membrane proteins diverge in their breakdown pattern. Figure 2
presents Western blots of a chlorophyll-binding thylakoid protein (LHCP2) and a typical soluble protein (GSAAT) from senescing leaf tissues of wild-type and stay-green introgression lines of L. temulentum. As described below, the latter genotype has a specific defect in the chlorophyll catabolism pathway. Degradation of soluble protein during senescence (exemplified by GSAAT) is close to normal. On the other hand membrane (light-harvesting and reaction centre) proteins are much more stable. Similar observations were made on stay-green lines of Phaseolus vulgaris (Bachmann et al., 1994). In vitro experiments show that when pigment-binding proteins are not properly complexed with chlorophyll they are more vulnerable to proteolytic attack. One explanation for this is that the pigment facilitates protein folding so that the most resistant peptide regions are on the outside of the molecule. The behaviour of pigment metabolism mutants is consistent with a similar function for chlorophyll as a protein protectant in vivo (Thomas, 1997).
|
The pigment proteolipids of thylakoids have both a photosynthetic function and a role in membrane structure (Allen and Forsberg, 2001
). Stabilizing chlorophyll–protein complexes in senescence has the effect of stabilizing membrane structure too. This in turn may reduce the lability of membrane-associated components that are not themselves directly stabilized by chlorophyll. An example of this is cytochrome f in chlorophyll catabolism mutants (Davies et al., 1990a, b; Bachmann et al., 1994). It also seems that a fraction of Rubisco that associates with the thylakoid can escape the fate of most other stroma proteins in such plants (Davies et al., 1990b). Conversely, part of a thylakoid intrinsic protein that extends into the stroma beyond the proteolytic no-go zone may be removed in non-yellowing mutants (Thomas and Howarth, 2000).
In the network of processes that regulate protein mobilization in senescence (Thomas and Donnison, 2000; Dangl et al., 2000), the induction of chlorophyll degradation is an early and, for membrane polypeptides, essential event. Genes for the chlorophyll pathway and its control are therefore important in the regulation of protein mobilization. Chlorophyll catabolism is summarized in Fig. 3. The genes for three steps in the pathway have been cloned—chlorophyllase (Jakob-Wilk et al., 1999; Tsuchiya et al., 1999), RCC reductase (Wüthrich et al., 2000) and the ABC-type tonoplast transporter (Lu et al., 1998; Tommasini et al., 1998). Mach et al. cloned the ACD2 locus of Arabidopsis and found it to be identical with RCC reductase (Mach et al., 2001). The knockout has an accelerated cell death phenotype, taking the form of light-dependent spreading lesions, with no evidence of stay-green-type behaviour. The gene responsible for the non-yellowing phenotype in grasses and legumes has not yet been cloned but a fair amount is known about it. The rest of this paper will review the gene in Festuca–Lolium and will describe approaches to isolating it.
|
|
Stay-green Festuca pratensis |
|---|
|
TopAbstractIntroductionStay-green Festuca pratensisChlorophyll metabolism in stay...Genes expressed in stay-green...ConclusionReferences |
|---|
The non-yellowing trait in Festuca pratensis was shown to be inherited as a simple Mendelian recessive (Thomas, 1987
). Superficially the phenotype seems to take the form of a more or less complete suppression of leaf senescence. Detailed comparison of leaves of the mutant with those of normally yellowing wild-type revealed the mutation to have interfered selectively with senescence processes. Total pigment levels decrease very little (but the complement of chlorophylls and their derivatives is altered in a characteristic way that is described later). Photosynthetic capacity diminishes more or less normally and the chlorophyll/Pmax relationship of the mutant is very different from the wild type (Hauck et al., 1997). The degradation of Rubisco and enhanced relative stability of chlorophyll-binding and other membrane-associated proteins are characteristic of senescence in the mutant (Thomas, 1987; Nock et al., 1992). These features contribute to distinctive ultrastructural qualities (Thomas, 1977). Plastoglobuli in plastids of stay-green F. pratensis are less electron dense than in the wild type and their accumulation during senescence is much reduced. Thylakoids of the mutant persist in gerontoplasts as loosely-appressed, but still recognizable, membrane structures. Immunolocalization shows persistence of LHCP2 and its randomization throughout the surviving degenerate thylakoids (Hilditch et al., 1989).
Special attributes of reproduction and genome organization in the two genera make species from the Lolium–Festuca complex particularly convenient subjects for introgression analysis. Introgression substitutes a gene by its homeologue from an alien background, allowing the locus to be identified, analysed and, ultimately, isolated. Species across the range of Lolium and Festuca are interfertile and homeologous chromosomes often pair and recombine freely (Canter et al., 1999). Recombination between Festuca and Lolium species is generally promiscuous, with rates of gene substitution reaching more than 70% in some crosses. DNA introgressed by interspecific or intergeneric hybridization in Lolium/Festuca is detectable by genomic in situ hybridization (GISH; Thomas et al., 1994) and by species-specific molecular markers (King et al., 1998). Lines of Lolium temulentum have been produced with and without the stay-green introgression from Festuca pratensis (Thomas et al., 1999).
|
Chlorophyll metabolism in stay-green Festuca/Lolium |
|---|
|
TopAbstractIntroductionStay-green Festuca pratensisChlorophyll metabolism in stay...Genes expressed in stay-green...ConclusionReferences |
|---|
Pigment metabolism in senescing leaves of Festuca and Lolium plants homozygous for the stay-green mutation is clearly disturbed. Chlorophyll a and total carotenoid levels are more or less stable during senescence, but chlorophyll b is almost as labile as it is in the wild type (Fig. 4
). Dephytylated, more polar derivatives, largely chlorophyllide and phaeophorbide, accumulate in the mutant, but are virtually undetectable in the wild type (Thomas et al., 1989). Assay of chlorophyllase, dechelatase, phaeophorbide a oxygenase (PaO), and red chlorophyll catabolite reductase (RCCR) show that PaO activity is missing in the mutant (Vicentini et al., 1995). The pigment phenotype is consistent with a blockage at PaO to RCC, resulting in progressive accumulation of proximal upstream catabolites. It should be mentioned that there is no evidence for disturbed chlorophyll biosynthesis in the mutant. As Fig. 2b
demonstrates, chlorophyll biosynthetic enzymes, of which GSAAT is an example, are lost at normal rates during senescence.
|
) Controls; (
) treated with the inactive L-stereoisomer of MDMP; (
) treated with D-MDMP, an inhibitor of cytoplasmic protein synthesis. Error bars give standard deviations (n=4).Protein synthesis inhibitors prevent yellowing in senescing wild-type leaves. They also stop the pigment changes occurring in the stay-green mutant (Fig. 4
). These data show that protein synthesis inhibitors act at two points in chlorophyll catabolism (Fig. 3). One is in the chlorophyll b to a conversion. Scheumann et al. showed that chlorophyll b reductase activity increased several-fold during senescence of barley leaves (Scheumann et al., 1999). The response to translation inhibitor suggests that at least one of the two enzymes carrying out this conversion is synthesized de novo. The other point of inhibition is in the catabolic sequence from chlorophyll a to non-fluorescent chlorophyll catabolites (NCCs). No evidence was found for inhibitor-sensitive synthesis of chlorophyllase during senescence in Lolium. Chlorophyllase gene expression has been observed to be constitutive in a range of tissues, though ethylene and jasmonate had some modulating influence (Jakob-Wilk et al., 1999; Tsuchiya et al., 1999). Dechelatase (Langmeier et al., 1993) and RCCR (Wüthrich et al., 2000) are also constitutive. All the evidence points to PaO as the only enzyme in the chlorophyll a catabolic pathway to be de novo synthesized in senescence (Hörtensteiner et al., 1995) and the likely step at which translation inhibitors intervene (Rodoni et al., 1998). The phenotype of the stay-green F. pratensis and Lolium introgressions is consistent with a PaO knockout (Vicentini et al., 1995). The mutation may therefore be located in the PaO gene, or a specific regulator of it. Cloning the stay-green locus would give a gene with an important role in the internal N economy of green plants.
|
Genes expressed in stay-green Festuca/Lolium |
|---|
|
TopAbstractIntroductionStay-green Festuca pratensisChlorophyll metabolism in stay...Genes expressed in stay-green...ConclusionReferences |
|---|
Over recent years, differential and subtractive cloning has resulted in the isolation of large numbers of genes with senescence-enhanced expression patterns from a range of species (Buchanan-Wollaston, 1997
; Dangl et al., 2000). Genes cloned from senescing leaves typically comprise a high proportion of sequences without a functional database match. For example, more than 2000 senescence-enhanced cDNAs (Sees) have been isolated from maize. Of those sequenced, more than three-quarters are unique sequences and more than half have no significant database similarity. On the basis of such figures, it is quite likely that the wild-type gene corresponding to the Festuca stay-green locus is somewhere in one or more of the existing collections of senescence-related cDNAs. The problem is one of recognizing it in the absence of a clear functional handle. The unique features of introgression in Lolium-Festuca have been exploited to narrow the options and close in on the region of the genome that the stay-green locus occupies.
As well as promiscuous alien recombination, there is a further experimental benefit of Lolium and Festuca for genetic analysis: a high degree of molecular polymorphism between the species and genera. This is reflected not only in genomic sequences at given loci, but also in expressed genes. Expressed genes carried on an introgressed segment can be identified as species-specific polymorphisms in corresponding cDNAs. An example is UDP-glucose pyrophosphorylase (UDPGP). The stay-green gene from F. pratensis was transferred to L. temulentum Ceres and the alien segment reduced by several backcrosses (Thomas et al., 1999). Figure 5a shows that the small introgressed segment carrying the F. pratensis stay-green gene is located at the extreme end of one of the L. temulentum chromosomes. Genes expressed in wild-type and stay-green Ceres were compared by cDNA-RDA. Several differentially expressed genes were identified (Thomas et al., 1997) including one which, when sequenced, showed a good match to barley UDPGP (Fig. 5b, c). The same gene cloned independently from several stay-green and wild-type individuals showed distinctive phenotype-specific single nucleotide polymorphisms. In each of the sequences from F. pratensis (wild type or stay-green) and from stay-green L. temulentum, the nucleotides at positions 160, 450 and 458 are A, C and T, respectively. At the same positions in all sequences from wild-type L. temulentum G, T and G occur. Thus the UDPGP gene of L. temulentum plants carrying the single F. pratensis segment (Fig. 5a) is clearly a Festuca gene. It means that UDPGP is a gene linked closely to stay-green that has travelled all the way to L. temulentum Ceres on the same F. pratensis-derived alien segment. Other genes of similar origin will undoubtedly be identified within the collections of stay-green or wild-type-specific polymorphic fragments isolated by cDNA-AFLP (Table 1) and by cDNA-RDA (Thomas et al., 1997). For the purpose of seeking transcripts corresponding to the stay-green locus, introgression limits the numbers of candidates to those genes located on a small alien segment. Systematic functional testing, including complementation in transgenic Lolium–Festuca, thus becomes feasible. At the very least this approach generates several polymorphic markers close to the stay-green locus. Applied to a large-insert genomic library from F. pratensis (I Donnison and I King, unpublished results) together with genomic tags such as AFLPs and microsatellites, these open up the prospect of gene isolation by chromosome landing.
|
|
|
Conclusion |
|---|
|
TopAbstractIntroductionStay-green Festuca pratensisChlorophyll metabolism in stay...Genes expressed in stay-green...ConclusionReferences |
|---|
The stay-green gene from Festuca pratensis, and similar (homologous?) genes from other species including Pisum sativum (Thomas et al., 1996
) and Phaseolus vulgaris (Ronning et al., 1991; Bachmann et al., 1994), profoundly influence the catabolism of both chlorophyll and protein during leaf senescence. Ever-closer cDNA and genomic tags for the F. pratensis stay-green locus have been identified. An F. pratensis BAC library is available. There is now detailed knowledge of the cellular and biochemical phenotype of stay-greens (Thomas and Howarth, 2000). For functional testing, efficient homologous transformation systems are available in Festuca and Lolium species (Dalton et al., 1999). Genomics resources in read-across models, notably maize, are directly accessible. It adds up to a set of powerful tools to isolate and characterize stay-green, which in turn will establish a crucial part of the regulatory mechanism for the internal N economy of plants.
|
Acknowledgments |
|---|
We are grateful to Barbara Hauck, Caron James, Ann Thomas, John Harper, and Gareth Morgan for their contributions to the work described here, and to Neil Jones for making Peter Canter's participation possible. The Institute of Grassland and Environmental Research is sponsored by the UK Biotechnology and Biological Sciences Research Council.
|
Notes |
|---|
1 To whom correspondence should be addressed. Fax: +44 (0)1970 823242. E-mail: sid.thomas{at}bbsrc.ac.uk
|
References |
|---|
|
TopAbstractIntroductionStay-green Festuca pratensisChlorophyll metabolism in stay...Genes expressed in stay-green...ConclusionReferences |
|---|
Allen JF, Forsberg J. 2001. Molecular recognition in thylakoid structure and function. Trends in Plant Science 6, 317–326.[Web of Science][Medline]
Bachmann A, Fernandez-Lopez J, Ginsburg S, Thomas H, Bouwkamp JC, Solomos T, Matile P. 1994. Stay-green genotypes of Phaseolus vulgaris L.—chloroplast proteins and chlorophyll catabolites during foliar senescence. New Phytologist 126, 593–600.
Buchanan-Wollaston V. 1997. The molecular biology of leaf senescence. Journal of Experimental Botany 48, 181–199.
Canter PH, Pasakinskiene I, Jones RN, Humphreys MW. 1999. Chromosome substitutions and recombination in the amphiploid Lolium perennexFestuca pratensis cv. Prior (2n=4x=28). Theoretical and Applied Genetics 98, 809–814.
Dalton SJ, Bettany AJE, Timms EJ, Morris P. 1999. Co-transformed, diploid Lolium perenne (perennial ryegrass), Lolium multiflorum (Italian ryegrass) and Lolium temulentum (Darnel) plants produced by microprojectile bombardment. Plant Cell Reports 18, 721–726.
Dangl JL, Dietrich RA, Thomas H. 2000. Senescence and programmed cell death. In: Buchanan B, Gruissem W, Jones R, eds. Biochemistry and molecular biology of plants. Rockville: ASPP, 1044–1100.
Davies TGE, Thomas H, Rogers LJ. 1990a. Immunological quantification of cytochrome f in leaves of a non-yellowing senescence mutant of Festuca pratensis. Photosynthesis Research 24, 99–108.
Davies TGE, Thomas H, Thomas BJ, Rogers LJ. 1990b. Leaf senescence in a non-yellowing mutant of Festuca pratensis: metabolism of cytochrome f. Plant Physiology 93, 588–595.
Feller U, Fischer A. 1994. Nitrogen metabolism in senescing leaves. Critical Reviews in Plant Science 13, 241–273.
Hauck B, Gay AP, Macduff J, Griffiths CM, Thomas H. 1997. Leaf senescence in a non-yellowing mutant of Festuca pratensis: implications of the stay-green mutation for photosynthesis, growth and nitrogen nutrition. Plant Cell and Environment 20, 1007–1018.
Hilditch P, Thomas H, Thomas BJ, Rogers LJ. 1989. Leaf senescence in a non-yellowing mutant of Festuca pratensis: proteins of Photosystem II. Planta 177, 265–272.[Web of Science]
Hörtensteiner S, Vicentini F, Matile P. 1995. Chlorophyll breakdown in senescent cotyledons of rape, Brassica napus L.: enzymatic cleavage of phaeophorbide a in vitro. New Phytologist 129, 237–246.
Jakob-Wilk D, Holland D, Goldschmidt EE, Riov J, Eyal Y. 1999. Chlorophyll breakdown by chlorophyllase: isolation and functional expression of the Chlase 1 gene from ethylene-treated Citrus fruit and its regulation during development. The Plant Journal 20, 653–661.[Web of Science][Medline]
King IP, Morgan WG, Armstead IP, Harper JA, Hayward MD, Bollard A, Nash JV, Forster JW, Thomas HM. 1998. Introgression mapping in the grasses. I. Introgression of Festuca pratensis chromosomes and chromosome segments into Lolium perenne. Heredity 81, 462–467.
Langmeier M, Ginsburg S, Matile P. 1993. Chlorophyll breakdown in senescent leaves: demonstration of Mg-dechelatase activity. Physiologia Plantarum 89, 347–353.
Lu Y-P, Li Z-S, Drozdowicz Y-M, Hörtensteiner S, Martinoia E, Rea PA. 1998. AtMRP2, an Arabidopsis ATP binding cassette transporter able to transport glutathione S-conjugates and chlorophyll catabolites: functional comparisons with AtMRP1. The Plant Cell 10, 267–282.
Mach JM, Castillo A, Hoogstraten R, Greenberg JT. 2001. The Arabidopsis accelerated cell death gene ACD encodes red chlorophyll catabolite reductase and suppresses the spread of disease symptoms. Proceedings of the National Academy of Sciences, USA 98, 771–776.
Matile P, Hörtensteiner S, Thomas H. 1999. Chlorophyll degradation. Annual Review of Plant Physiology and Plant Molecular Biology 50, 67–95.[Web of Science]
Nock LP, Rogers LJ, Thomas H. 1992. Metabolism of protein and chlorophyll in leaf tissue of Festuca pratensis Huds. during chloroplast assembly and senescence. Phytochemistry 31, 1465–1470.
Rodoni S, Schellenberg M, Matile P. 1998. Chlorophyll breakdown in senescing barley leaves as correlated with pheophorbide a oxygenase activity. Journal of Plant Physiology 152, 139–144.
Ronning CM, Bouwkamp JC, Solomos T. 1991. Observations on the senescence of a mutant non-yellowing genotype of Phaseolus vulgaris L. Journal of Experimental Botany 42, 235–241.
Scheumann V, Schoch S, Rüdiger W. 1999. Chlorophyll b reduction during senescence of barley seedlings. Planta 209, 364–370.[Web of Science][Medline]
Thomas H. 1977. Ultrastructure, polypeptide composition and photochemical activity of chloroplasts during foliar senescence of a non-yellowing mutant genotype of Festuca pratensis Huds. Planta 137, 53–60.[Web of Science]
Thomas H. 1987. Sid: a Mendelian locus controlling thylakoid membrane disassembly in senescing leaves of Festuca pratensis. Theoretical and Applied Genetics 73, 551–555.
Thomas H. 1997. Chlorophyll: a symptom and a regulator of plastid development. New Phytologist 136, 163–181.
Thomas H, Bortlik K, Rentsch D, Schellenberg M, Matile P. 1989. Catabolism of chlorophyll in vivo: significance of polar chlorophyll catabolites in a non-yellowing senescence mutant of Festuca pratensis. New Phytologist 111, 3–8.[Web of Science]
Thomas H, Donnison I. 2000. Back from the brink: plant senescence and its reversibility. In: Bryant J, Hughes SG, Garland JM, eds. Programmed cell death in animals and plants. Oxford: Bios, 149–162.
Thomas H, Evans C, Thomas HM, Humphreys MW, Morgan WG, Hauck B, Donnison I. 1997. Introgression, tagging and expression of a leaf senescence gene in Festulolium. New Phytologist 137, 29–34.
Thomas H, Howarth CJ. 2000. Five ways to stay green. Journal of Experimental Botany 51, 329–337.
Thomas H, Morgan WG, Thomas AM, Ougham HJ. 1999. Expression of the stay-green character introgressed into Lolium temulentum Ceres from a senescence mutant of Festuca pratensis. Theoretical and Applied Genetics 99, 92–99.
Thomas H, Schellenberg M, Vicentini F, Matile P. 1996. Gregor Mendel's green and yellow pea seeds. Botanica Acta 109, 3–4.[Web of Science]
Thomas HM, Morgan WG, Meredith MR, Humphreys MW, Thomas H, Leggett JM. 1994. Identification of parental and recombined chromosomes of Lolium multiflorumxFestuca pratensis by genomic in situ hybridization. Theoretical and Applied Genetics 88, 909–913.
Tommasini R, Vogt E, Fromenteau M, Hörtensteiner S, Matile P, Amrhein N, Martinoia E. 1998. An ABC transporter of Arabidopsis thaliana has both glutathione-conjugate and chlorophyll catabolite transport activity. The Plant Journal 13, 773–780.[Web of Science][Medline]
Tsuchiya T, Ohta H, Okawa K, Iwamatsu A, Shimada H, Masuda T, Takamiya K. 1999. Cloning of chlorophyllase, the key enzyme in chlorophyll degradation: finding of a lipase motif and the induction by methyl jasmonate. Proceedings of the National Academy of Sciences, USA 96, 15362–15367.
Vicentini F, Hörtensteiner S, Schellenberg M, Thomas H, Matile P. 1995. Chlorophyll breakdown in senescent leaves: identification of the biochemical lesion in a stay-green genotype of Festuca pratensis Huds. New Phytologist 129, 247–252.[Web of Science]
Wüthrich KL, Bovet L, Hunziker PE, Donnison IS, Hörtensteiner S. 2000. Molecular cloning, functional expression and characterisation of RCC reductase involved in chlorophyll catabolism. The Plant Journal 21, 189–198.[Web of Science][Medline]
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  E. Alos, M. Roca, D. J. Iglesias, M. I. Minguez-Mosquera, C. M. B. Damasceno, T. W. Thannhauser, J. K. C. Rose, M. Talon, and M. Cercos An Evaluation of the Basis and Consequences of a Stay-Green Mutation in the navel negra Citrus Mutant Using Transcriptomic and Proteomic Profiling and Metabolite Analysis Plant Physiology, July 1, 2008; 147(3): 1300 - 1315. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 U. Feller, I. Anders, and T. Mae Rubiscolytics: fate of Rubisco after its enzymatic function in a cell is terminated J. Exp. Bot., May 1, 2008; 59(7): 1615 - 1624. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S.-Y. Park, J.-W. Yu, J.-S. Park, J. Li, S.-C. Yoo, N.-Y. Lee, S.-K. Lee, S.-W. Jeong, H. S. Seo, H.-J. Koh, et al. The Senescence-Induced Staygreen Protein Regulates Chlorophyll Degradation PLANT CELL, May 1, 2007; 19(5): 1649 - 1664. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Wingler, E. Brownhill, and N. Pourtau Mechanisms of the light-dependent induction of cell death in tobacco plants with delayed senescence J. Exp. Bot., November 1, 2005; 56(421): 2897 - 2905. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. Tanaka, M. Hirashima, S. Satoh, and A. Tanaka The Arabidopsis-accelerated cell death Gene ACD1 is Involved in Oxygenation of Pheophorbide a: Inhibition of the Pheophorbide a Oxygenase Activity does not Lead to the "Stay-Green" Phenotype in Arabidopsis Plant Cell Physiol., December 15, 2003; 44(12): 1266 - 1274. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. J.M. Clerkx, H. B.-D. Vries, G. J. Ruys, S. P.C. Groot, and M. Koornneef Characterization of green seed, an Enhancer of abi3-1 in Arabidopsis That Affects Seed Longevity Plant Physiology, June 1, 2003; 132(2): 1077 - 1084. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||