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First published online March 21, 2008; 10.1104/pp.108.118430 Plant Physiology 147:179-187 (2008) © 2008 American Society of Plant Biologists OPEN ACCESS ARTICLE
Amino Acid Substitutions in Homologs of the STAY-GREEN Protein Are Responsible for the green-flesh and chlorophyll retainer Mutations of Tomato and Pepper1,[W],[OA]Department of Horticulture, Michigan State University, East Lansing, Michigan 48824 (C.S.B.); Boyce Thompson Institute for Plant Research, Ithaca, New York 14853 (C.S.B., R.P.M., M.-Y.C., A.B., J.J.G.); and U.S. Department of Agriculture Agricultural Research Service, Plant, Soil and Nutrition Laboratory, Ithaca, New York 14853 (R.P.M., J.J.G.)
Color changes often accompany the onset of ripening, leading to brightly colored fruits that serve as attractants to seed-dispersing organisms. In many fruits, including tomato (Solanum lycopersicum) and pepper (Capsicum annuum), there is a sharp decrease in chlorophyll content and a concomitant increase in the synthesis of carotenoids as a result of the conversion of chloroplasts into chromoplasts. The green-flesh (gf) and chlorophyll retainer (cl) mutations of tomato and pepper, respectively, are inhibited in their ability to degrade chlorophyll during ripening, leading to the production of ripe fruits characterized by both chlorophyll and carotenoid accumulation and are thus brown in color. Using a positional cloning approach, we have identified a point mutation at the gf locus that causes an amino acid substitution in an invariant residue of a tomato homolog of the STAY-GREEN (SGR) protein of rice (Oryza sativa). Similarly, the cl mutation also carries an amino acid substitution at an invariant residue in a pepper homolog of SGR. Both GF and CL expression are highly induced at the onset of fruit ripening, coincident with the ripening-associated decline in chlorophyll. Phylogenetic analysis indicates that there are two distinct groups of SGR proteins in plants. The SGR subfamily is required for chlorophyll degradation and operates through an unknown mechanism. A second subfamily, which we have termed SGR-like, has an as-yet undefined function.
Color change is one of the most dramatic events occurring in fleshy fruits as they begin to ripen, serving as a signal to seed-dispersing fauna that the fruit is ripe, palatable, and nutritious. Fleshy fruits predominantly accumulate carotenoids, anthocyanins, and flavanoids, and the de novo synthesis of these compounds at the onset of ripening is preceded by, or occurs concomitantly with, the degradation of chlorophyll (Seymour et al., 1993  ). An exception to this generalization occurs in banana (Musa spp.), where the degradation of chlorophyll at the onset of ripening leads to the unmasking of the yellow-pigmented xanthophylls that are already present in immature fruit (Seymour et al., 1993; Drury et al., 1999). Therefore, whereas the degradation of chlorophyll is one of the key events accompanying the reprogramming of cellular metabolism at the onset of fruit ripening, these two events are not necessarily interdependent. While mechanisms of chlorophyll degradation have been elucidated, the regulation and role of chlorophyll degradation in the ripening process and overall quality of fruits remain poorly understood.
Chlorophyll degradation is a highly controlled sequential process that converts the fluorescent chlorophyll molecule into nonfluorescent catabolites that are stored within the vacuole. The basic chlorophyll breakdown pathway is composed of the following steps: chlorophyll b
Stay-green mutants have been identified in several plant species and classified on the basis of their chlorophyll retention and general senescence phenotypes (Thomas and Howarth, 2000
Fruit of the green-flesh (gf) mutant of tomato (Solanum lycopersicum) ripen to a muddy brown color due to the accumulation of lycopene coupled with a lack of chlorophyll degradation (Kerr, 1956 In this article, we describe the molecular identification of GF via the utilization of a positional cloning approach. Through DNA sequence analysis of the gf locus and complementation studies, we demonstrate unequivocally that GF is a member of the STAY-GREEN (SGR) gene family. In addition, we have demonstrated that a mutation in a pepper homolog of GF likely represents the basis for the stay-green phenotype of the pepper cl mutant.
Positional Cloning of GF
The gf locus has previously been mapped onto the classical genetic map of tomato at a position of approximately 45 cM on the long arm of chromosome 8 (Tanksley et al., 1992
As part of the international initiative to sequence the eukaryotic gene space of cultivated tomato, the sequence of numerous bacterial artificial chromosome (BAC) clones residing on chromosome 8 has been determined (http://www.sgn.cornell.edu/about/japan.pl), including the BAC clones LeHBa0165B06 and LeHBa0197J17 that contain the markers CT148 and CT265, respectively. In an effort to generate additional genetic markers between CT148 and CT265 to further our mapping effort, we investigated the structure of these sequenced BAC clones in more detail. The tomato genome-sequencing effort is utilizing a BAC-by-BAC approach and a large number of BAC clones have been genetically fingerprinted and assembled into contigs. Analysis of LeHBA0165B06 revealed that Finger Print Contig analysis had placed this clone within a contig containing three additional BAC clones, LeHBa0004P13, LeHBa0020K14, and LeHBA0066O08 (http://www.genome.arizona.edu/fpc/tomato). We investigated the homologies of the BAC end sequences of these additional clones using the BLASTN tool of the SOL Genomics Network (SGN) to search against the entire collection of Solanaceae unigenes. This analysis revealed that the LeHBa0020K14-T7 BAC end was identical to a region of SGN-U316068. This unigene comprises 26 EST reads and is annotated as the senescence-inducible SGR1 protein of tomato, which is in turn a homolog of the SGR protein of rice (Park et al., 2007
Given the homology of SGN-U316068 and its tight linkage to gf, we reasoned that this would be a strong candidate for GF. Amplification of the corresponding full-length cDNA of SGN-U316068 from GF/GF and gf/gf genetic backgrounds and subsequent sequence analysis of the cloned products revealed a single A  T nucleotide change at position 429 of the predicted coding sequence in the gf/gf mutant. This nucleotide change converts amino acid 143 from an Arg to a Ser in the gf/gf mutant background.
The open reading frame (ORF) of SGN-U316068 amplified from the wild-type (GF/GF) background was inserted downstream of the cauliflower mosaic virus (CaMV) 35S promoter in the binary vector pBI121 that had first been modified to remove the GUS reporter gene. This construct was introduced into the gf/gf mutant background via Agrobacterium-mediated transformation. Seventeen primary transformants were recovered that displayed ripe fruits that were red in color rather than the typical brown color associated with the gf mutation, suggesting that SGN-U316068 was able to complement the mutant phenotype. Genetic complementation was confirmed in segregating T1 progeny. Three independent T1 lines were selected and screened by Southern analysis for the presence or absence of the transgene (data not shown). Fruit from plants that contained the transgene were red, whereas plants that had segregated out the transgene produced brown fruit characteristic of the gf parent (Fig. 2A
). Tomato leaves from plants exposed to nutrient stress or detached leaves that have been placed in the dark readily lose chlorophyll and this loss is inhibited in the gf mutant (Akhtar et al., 1999
Sequence Analysis of the cl Locus
Following confirmation that we had cloned the gene responsible for conferring the gf mutation and that it was indeed located within the corresponding genomic interval as the cl locus, we utilized the predicted GF amino acid sequence to search the pepper gene indices (http://compbio.dfci.harvard.edu/tgi/plant.html) for a homologous gene that might serve as a candidate for CL. We identified a single contig of six EST clones (TC4187) that were predicted to encode a pepper protein of 266 amino acids that shared 86% amino acid identity over its entire length to GF. Primers were designed to PCR amplify the entire ORF from cDNA synthesized from RNA isolated from red (CL/CL) and brown (cl/cl) fruited peppers. A single amplification product was obtained from each genotype and these were cloned and sequenced. The nucleotide sequence of the cDNA clones amplified from CL/CL was identical to the sequence of the TC4187 consensus sequence. However, the cDNA clones derived from the cl/cl fruit contained a single T
In silico analysis of EST data indicated that the transcripts of both GF and CL were likely to increase in abundance at the onset of fruit ripening in tomato and pepper. The tomato unigene SGN-U316068 is composed of 26 individual EST reads, of which 24 are derived from cDNA libraries prepared from RNA extracted from either ripening fruit or from mixed pools of fruit at different stages of development. The remaining two ESTs are derived from undifferentiated callus and anthesis staged flower cDNA libraries. The consensus sequence TC4187 that corresponds to the pepper CL gene contains only six individual EST reads, but all are derived from RNA isolated from red-ripe pepper fruit. We determined the expression of both GF and CL during fruit development and ripening in both tomato and pepper (Fig. 3 ). Transcripts were low or undetectable in green fruit, but showed increased abundance at the onset of ripening in both species. In addition, we monitored the expression of both GF and CL in the gf and cl mutant backgrounds to ascertain whether the mutations impacted the expression of either gene. There was no significant difference in transcript abundance detected between wild-type and mutant fruit for either GF or CL, suggesting that the absence of chlorophyll degradation does not influence the expression of these genes.
GF and CL Represent New Members of the SGR Gene Family Through a combination of positional cloning and candidate gene analysis, we have identified single-nucleotide changes that define the mutations at the gf and cl loci of tomato and pepper. These mutations arise in orthologs of the rice SGR gene. The SGR family is conserved in plants and distant homologs are present in algae and, unexpectedly, in species of Bacillus and Clostridium, but not in other bacterial genomes. To investigate the relationship of this family, we collected predicted full-length sequences from GenBank and other family and organism-specific databases and performed a phylogenetic analysis using the predicted protein sequences (Fig. 4 ). The data clearly indicate that there are two clades that represent distinct subfamilies of these genes in plants. The family highlighted by the gray box most likely represents genes that are functionally equivalent to SGR and contains several members that have been shown through mutational analysis to be involved in chlorophyll degradation, including family members from Arabidopsis, rice, and pea, as well as GF and CL. These proteins range from approximately 260 to 295 amino acids in length. They have a highly conserved central core that displays between 70% and 95% amino acid identity to the GF protein, but are fairly divergent at both their N and C termini. This divergence is particularly apparent between proteins from different plant families. Within this SGR subfamily, some species, such as Arabidopsis, soybean (Glycine max), corn, and Physcomitrella patens contain paralogous genes, although we have not uncovered any evidence of this within the Solanaceae. In addition, a second distinct subfamily is evident in plants that contains members of several plant families and includes homologs from rice and Arabidopsis. The proteins within this subfamily are between 251 and 260 amino acids and are more distantly related to GF, sharing approximately 50% amino acid identity within the central core of the protein. To date, no mutant phenotypes have been assigned to any of the members of this subfamily, but, like the SGR subfamily, using both the TargetP (http://www.cbs.dtu.dk/services/TargetP) and Predotar (http://urgi.versailles.inra.fr/predotar/predotar.html) prediction servers, all are predicted to encode proteins that are targeted to the chloroplast.
The mutations at the gf and cl loci result in the amino acid substitutions R143S and W114R, respectively. An amino acid alignment of GF and CL, together with representative proteins from each family subgroup, indicated that Arg-143 and Trp-114 represent invariant residues within the SGR family (Fig. 5 ). This observation was found to hold true even within a group of nine proteins from various Clostridium and Bacillus species (data not shown). From the various mutant loci described to date within the SGR family, two mutant alleles in rice SGR also result in amino acid substitutions that convert Y84C and V99M (Jiang et al., 2007 ; Park et al., 2007). Our alignments showed that Tyr-84 also represents a completely conserved residue in all the protein sequences that we recovered from database searches and that Val-99 is substituted in about 50% of the proteins for an Ile residue, but that no other amino acid occurs at this position (Fig. 5). These conserved residues are all located within the central core of this protein family, toward the N terminus of the mature protein, suggesting that this region of the protein is important for function.
Stay-green mutants have been identified in an array of plant species. The gf and cl mutants of tomato and pepper display a stay-green phenotype that leads to the production of brown fruits as the result of carotenoid accumulation and lack of chlorophyll degradation. Through a combination of genetic mapping and candidate gene analysis, we have provided strong evidence indicating that the stay-green phenotypes of the gf and cl loci are the result of single amino acid substitutions in orthologs of the recently identified SGR gene of rice (Park et al., 2007 ). The SGR gene family is required for chlorophyll degradation and, in addition to rice SGR, mutant alleles that display stay-green phenotypes have been identified in Arabidopsis, pea, and F. pratensis (Armstead et al., 2006, 2007; Ren et al., 2007; Sato et al., 2007).
Mutations in the SGR gene family have been designated as class C stay-green mutants that are deficient in their ability to break down chlorophyll, but have an otherwise normal pattern of senescence (Thomas and Howarth, 2000
Our phylogenetic analysis indicates that there are two subfamilies of SGR-like proteins in plants (Fig. 4A). This conclusion is similar to that obtained in a recently published study of the SGR family (Aubry et al., 2008
Overexpression of SGR in rice and Arabidopsis yielded plants that produced leaves with pale phenotypes or plants that died following transfer from tissue culture (Jiang et al., 2007
Chlorophyll degradation and the transition of chloroplasts into chromoplasts represent a dramatic change in metabolism at the onset of fruit ripening. However, little is known about the role of chlorophyll degradation and the regulation of this pathway during the ripening process, nor the overall contribution that it makes to fruit quality. In both the gf and cl mutants, the thylakoid membranes persist during fruit ripening, leading to the occurrence of both thylakoids and plastoglobuli within the plastids (Cheung et al., 1993
With the exception of CHLOROPHYLLASE, few expression data are available for genes involved in the chlorophyll degradation pathway during the ripening of fleshy fruits. CHLOROPHYLLASE transcripts were found to be of low abundance and constitutively expressed during natural ripening in citrus, but expression and enzyme activity could be stimulated by ethylene treatment (Jacob-Wilk et al., 1999 The gf and cl mutations are used in commercial breeding lines of tomato and pepper and the gf mutation likely forms the genetic basis for several heirloom tomato varieties that have names typically associated with the colors black and purple, including, among others, Carbon, Black Krim and Purple Passion. Defining the molecular basis of both the gf and cl mutations provides genetic markers that can be utilized to select these traits early during breeding programs and to clearly define the genetic basis of the multitude of heirloom tomato varieties that display phenotypic similarity to the gf mutation. The chlorophyll degradation pathway has been extensively studied in leaves, where it forms an integral component of the senescence process because the nutrients are recycled at a particular stage in the plant's life cycle or in response to environmental challenges. In contrast, in fleshy fruits, such as tomato and pepper, chlorophyll degradation accompanies the onset of fruit ripening and the associated conversion of chloroplasts to chromoplasts marks a brief period of high metabolic activity leading to the synthesis of a range of compounds that serve as attractants for seed-dispersing animals. Identification of the molecular basis of the gf and cl mutations has revealed novel alleles in SGR orthologs that will aid functional studies of this protein family and provides tools for comparing the regulation of chlorophyll degradation between vegetative and reproductive tissues together with the influence of this process on fruit quality.
Plant Material and Growth Treatments Tomato (Solanum lycopersicum) seeds homozygous for the gf mutation (LA3534) and the Solanum pennellii introgression lines IL8-2 (LA4074) and IL8-3 (LA4076) were obtained from the Tomato Genetics Resource Center, University of California, Davis. The parental cultivar Ailsa Craig was originally obtained from the Glasshouse Crops Research Institute (Littlehampton, Sussex, UK). Pepper (Capsicum annuum) seeds of the Ancho type that were either red fruited (CL/CL) or brown fruited (cl/cl) were provided by Dr. S. Moore and Dr. M. Jahn, Department of Plant Breeding, Cornell University. Plants were grown in peat-based compost supplemented with fertilizer in greenhouses equipped with heating and cooling systems and supplemental lighting either at Cornell University (Ithaca, NY) or Michigan State University (East Lansing, MI). Fruits for RNA extraction were harvested at the indicated stage of maturity with the term breaker being used to determine the onset of fruit ripening in both tomato and pepper. Seeds and locular gel were removed and the pericarp frozen in liquid nitrogen and stored at –80°C until use. The leaf degreening assay was performed by harvesting expanding terminal leaflets from the fourth true leaf of young tomato plants prior to the onset of flowering. Leaves were excised and floated on water in sealed petri dishes. The dishes were wrapped in aluminum foil and placed in darkness for 2 weeks at room temperature.
Genomic DNA isolation was performed as described previously (Barry et al., 2005
Full-length cDNAs corresponding to the tomato unigene SGN-U316068 were amplified from breaker fruit cDNA synthesized from either the GF/GF or the gf/gf background using the primers U316068F (5'-GGACTTTTATCAAACAGCTAACTTGCA-3') and U316068R (5'-GGCACAACCCAACTTACAATAATTGTA-3'). Fragments were amplified using the Pfu Ultra DNA polymerase (Stratagene) and cloned using the Zero Blunt TOPO PCR cloning kit (Invitrogen). Full-length cDNA fragments, corresponding to the pepper homolog of SGR, were amplified from cDNA synthesized from pepper fruit RNA extracted at the breaker stage of development. The primer sequences PEPGF-F (5'-CACAACTCCTCTTTAAGTTTCTACTC-3') and PEPGF-R (5'-TCTTGCTTCCACAAACCCTATAATGA-3') were designed from the consensus contig TC4187 assembled in the pepper gene indices (http://compbio.dfci.harvard.edu/tgi/plant.html). Fragments were amplified from both red (CL/CL) and brown (cl/cl) fruited peppers using the FastStart high-fidelity PCR system (Roche Applied Science) and ligated into the pGEM-T Easy vector system (Promega). In both the tomato and pepper reverse transcription-PCR experiments, four clones were sequenced from each genetic background to confirm the existence of the genetic polymorphisms. Gene expression was determined using northern-blot analysis on total RNA extracted from fruit samples with full-length GF and CL as previously described (Griffiths et al., 1999
The full-length cDNA sequence of GF was reamplified from a cloned template using the primers GFCOMPF and GFCOMPR, which are identical to U316068F and U316068R, respectively, but with the addition of a BamHI linker on the forward primer and a SmaI restriction site on the reverse primer. This fragment was cloned using TOPO cloning as described above. The fragment was excised using the restriction enzyme sites in the linkers and ligated downstream of the CaMV 35S promoter in the binary vector pBI121, previously modified by removal of the UidA coding region by digestion with SacI followed by polishing with T4 DNA polymerase and subsequent BamHI digestion. Construct fidelity was confirmed by DNA sequencing. Transgenic tomato plants were generated through cotyledon-derived explants via Agrobacterium tumefaciens-mediated transformation (strain LBA4404), using previously described methods (Fillatti et al., 1987
DNA sequences were assembled using Sequencher Version 4.7 (Genecodes Corporation). Amino acid sequences were deduced from cDNA clones using ORF Finder (http://www.ncbi.nlm.nih.gov/gorf/gorf.html). Sequences used for comparisons and phylogenetic analysis were downloaded from organism-specific databases or from GenBank (http://www.ncbi.nlm.nih.gov/Genbank). The Arabidopsis (Arabidopsis thaliana) sequences At1g44000, At4g11910, and At4g22920 are based on The Arabidopsis Information Resource (TAIR) annotations (http://www.arabidopsis.org). The following sequences were obtained using their GenBank accession numbers: rice (Oryza sativa) SGR, EAZ09856; rice SGR-like (Os04g0692600), NP_001054370; soybean (Glycine max) SGR1, AAW82959; soybean SGR2, AAW82960; maize (Zea mays) SGR1, NP_001105770; maize SGR2, NP_001105771; sorghum (Sorghum bicolor) SGR, AAW82958; oat (Avena sativa) SGR, AAW82955; pea (Pisum sativum) SGR, BAF76351; tobacco (Nicotiana tabacum) SGR, ABY19382; Physcomitrella patens SGR1, EDQ70701; P. patens SGR2, EDQ62217; P. patens SGR-like, EDQ81746; Physcomitrella sitchensis SGR ABK22344; Ostreococcus tauri, CAL56489; and Clostridium botulinum, YP_001391480. The grape (Vitis vinifera) sequences are based upon annotation derived from a grape genome database (http://www.plantgdb.org/VvGDB/index.php) from the following sequence identifiers: grape SGR, PUT-157a-Vitis_vinifera-4592; and grape SGR-like, PUT-157a-Vitis_vinifera-43151296. Solanaceae SGR homologs were obtained from sequences deposited at SGN (http://www.sgn.cornell.edu) with the following unigene identifiers: potato (Solanum tuberosum) SGR, SGN-U272740; potato SGR-like, SGN-U274726; and tobacco SGR-like, SGN-U369489. Amino acid alignments were generated using either ClustalW or ClustalX and were decorated using the Boxshade server (Version 3.2.1; http://www.ch.embnet.org). Phylogenetic trees were constructed using the PHYLIP Version 3.67 suite of programs (http://evolution.genetics.washington.edu/phylip.html) and visualized using Treeview software. Sequence data from this article can be found in the GenBank/EMBL data libraries under accession numbers EU414631 (CL) and EU414632 (GF).
The following materials are available in the online version of this article.
Received February 26, 2008; accepted March 17, 2008; published March 21, 2008.
1 This work was supported by Michigan State University and the Michigan Agricultural Experiment Station (grant to C.B.), and National Science Foundation Plant Genome grants (grant nos. 05–01778 and 06–06595 to J.G.).  The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Cornelius S. Barry (barrycs{at}msu.edu).
[W] The online version of this article contains Web-only data.
[OA] Open Access articles can be viewed online without a subscription. www.plantphysiol.org/cgi/doi/10.1104/pp.108.118430 * Corresponding author; e-mail barrycs{at}msu.edu.
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