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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

The expression pattern of the Pho1a genes encoding plastidic starch phosphorylase correlates with the degradation of starch during fruit ripening in green-fruited and red-fruited tomato species

Maria A. Slugina https://orcid.org/0000-0003-1281-3837 A C , Anna V. Shchennikova A and Elena Z. Kochieva A B
+ Author Affiliations
- Author Affiliations

A Institute of Bioengineering, Research Centre of Biotechnology of the Russian Academy of Sciences, Leninsky prospect. 33, bld. 2, Moscow 119071, Russia.

B Lomonosov Moscow State University, GSP-1, Leninskie Gory, Moscow 119991, Russia.

C Corresponding author. Email: mashinmail@mail.ru

Functional Plant Biology 46(12) 1146-1157 https://doi.org/10.1071/FP18317
Submitted: 6 December 2018  Accepted: 17 July 2019   Published: 16 October 2019

Abstract

Genes encoding plastidic starch phosphorylase Pho1a were identified in 10 tomato species (Solanum section Lycopersicon). Pho1a genes showed higher variability in green-fruited than in red-fruited tomato species, but had an extremely low polymorphism level compared with other carbohydrate metabolism genes and an unusually low ratio of intron to exon single nucleotide polymorphisms (SNPs). In red-fruited species, Pho1a was expressed in all analysed tissues, including fruit at different developmental stages, with the highest level in mature green fruit, which is strong sink organ importing sucrose and accumulating starch. In green-fruited species Solanum peruvianum and Solanum arcanum, the Pho1a expression level was similar in mature green and ripe fruit, whereas in Solanum chmielewskii, it was higher in ripe fruit, and in Solanum habrochaites, the dynamics of fruit-specific Pho1a expression was similar to that in red-fruited tomatoes. During fruit development, in red-fruited Solanum lycopersicum, sucrose level was low, the monosaccharide content increased; in green-fruited S. peruvianum, the sucrose concentration increased and those of monosaccharides decreased. In both species, the starch content and Pho1a expression were downregulated. The evolutionary topology based on Pho1a sequences was consistent with the current division of tomatoes into red-fruited and green-fruited species, except for S. habrochaites.

Additional keywords: Pho1a, plastidic starch-phosphorylase, Solanum section Lycopersicon, starch metabolism, tomato species.


References

Albrecht T, Greve B, Pusch K, Kossmann J, Buchner P, Wobus U, Steup M (1998) Homodimers and heterodimers of Pho1-type phosphorylase isoforms in Solanum tuberosum L. as revealed by sequence-specific antibodies. European Journal of Biochemistry 251, 343–352.
Homodimers and heterodimers of Pho1-type phosphorylase isoforms in Solanum tuberosum L. as revealed by sequence-specific antibodies.Crossref | GoogleScholarGoogle Scholar | 9492303PubMed |

Albrecht T, Koch A, Lode A, Greve B, Schneider-Mergener J, Steup M (2001) Plastidic (Pho1-type) phosphorylase isoforms in potato (Solanum tuberosum L.) plants: expression analysis and immunochemical characterization. Planta 213, 602–613.
Plastidic (Pho1-type) phosphorylase isoforms in potato (Solanum tuberosum L.) plants: expression analysis and immunochemical characterization.Crossref | GoogleScholarGoogle Scholar | 11556793PubMed |

Azanza F, Kim D, Tanksley SD, Juvik JA (1995) Genes from Lycopersicon chmielewskii affecting tomato quality during fruit ripening. Theoretical and Applied Genetics 91, 495–504.
Genes from Lycopersicon chmielewskii affecting tomato quality during fruit ripening.Crossref | GoogleScholarGoogle Scholar | 24169841PubMed |

Bailey TL, Elkan C (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers. In ‘Proceedings of the second international conference on intelligent systems for molecular biology’. pp. 28–36. (AAAI Press: Menlo Park, CA, USA)

Ball S, Morell MK (2003) From bacterial glycogen to starch: understanding the biogenesis of the starch granule. Annual Review of Plant Biology 54, 207–233.
From bacterial glycogen to starch: understanding the biogenesis of the starch granule.Crossref | GoogleScholarGoogle Scholar | 14502990PubMed |

Ball S, Colleoni C, Cenci U, Raj JN, Tirtiaux C (2011) The evolution of glycogen and starch metabolism in eukaryotes gives molecular clues to understand the establishment of plastid endosymbiosis. Journal of Experimental Botany 62, 1775–1801.
The evolution of glycogen and starch metabolism in eukaryotes gives molecular clues to understand the establishment of plastid endosymbiosis.Crossref | GoogleScholarGoogle Scholar | 21220783PubMed |

Barsan C, Zouine M, Maza E, Bian W, Egea I, Rossignol M, Bouyssie D, Pichereaux C, Purgatto E, Bouzayen M, Latché A, Pech JC (2012) Proteomic analysis of chloroplast-to-chromoplast transition in tomato reveals metabolic shifts coupled with disrupted thylakoid biogenesis machinery and elevated energy-production components. Plant Physiology 160, 708–725.
Proteomic analysis of chloroplast-to-chromoplast transition in tomato reveals metabolic shifts coupled with disrupted thylakoid biogenesis machinery and elevated energy-production components.Crossref | GoogleScholarGoogle Scholar | 22908117PubMed |

Beck E, Ziegler P (1989) Biosynthesis and degradation of starch in higher plants. Annual Review of Plant Physiology and Plant Molecular Biology 40, 95–117.
Biosynthesis and degradation of starch in higher plants.Crossref | GoogleScholarGoogle Scholar |

Beckles DM (2012) Factors affecting the postharvest sugar content of tomato Solanum lycopersicum L. fruit. Postharvest Biology and Technology 63, 129–140.
Factors affecting the postharvest sugar content of tomato Solanum lycopersicum L. fruit.Crossref | GoogleScholarGoogle Scholar |

Beckles DM, Hong N, Stamova L, Luengwilai K (2012) Biochemical factors contributing to tomato fruit sugar content: a review. Fruits 67, 49–64.
Biochemical factors contributing to tomato fruit sugar content: a review.Crossref | GoogleScholarGoogle Scholar |

Bemer M, Karlova R, Ballester AR, Tikunov YM, Bovy AG, Wolters-Arts M, de Barros Rossetto P, Angenent GC, de Maagd RA (2012) The tomato FRUITFULL homologs TDR4/FUL1 and MBP7/FUL2 regulate ethylene-independent aspects of fruit ripening. The Plant Cell 24, 4437–4451.
The tomato FRUITFULL homologs TDR4/FUL1 and MBP7/FUL2 regulate ethylene-independent aspects of fruit ripening.Crossref | GoogleScholarGoogle Scholar | 23136376PubMed |

Bertoni M, Kiefer F, Biasini M, Bordoli L, Schwede T (2017) Modeling protein quaternary structure of homo- and hetero-oligomers beyond binary interactions by homology. Scientific Reports 7, 10480
Modeling protein quaternary structure of homo- and hetero-oligomers beyond binary interactions by homology.Crossref | GoogleScholarGoogle Scholar | 28874689PubMed |

Biasini M, Bienert S, Waterhouse A, Arnold K, Studer G, Schmidt T, Kiefer F, Cassarino TG, Bertoni M, Bordoli L, Schwede T (2014) SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Research 42, W252–W258.
SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information.Crossref | GoogleScholarGoogle Scholar | 24782522PubMed |

Bienert S, Waterhouse A, de Beer TA, Tauriello G, Studer G, Bordoli L, Schwede T (2017) The SWISS-MODEL Repository – new features and functionality. Nucleic Acids Research 45, D313–D319.
The SWISS-MODEL Repository – new features and functionality.Crossref | GoogleScholarGoogle Scholar | 27899672PubMed |

Brisson N, Giroux H, Zollinger M, Camirand A, Simard C (1989) Maturation and subcellular compartmentation of potato starch phosphorylase. The Plant Cell 1, 559–566.

Camirand A, St-Pierre B, Marineau C, Brisson N (1990) Occurrence of a copia-like transposable element in one of the introns of the potato starch phosphorylase gene. Molecular & General Genetics 224, 33–39.
Occurrence of a copia-like transposable element in one of the introns of the potato starch phosphorylase gene.Crossref | GoogleScholarGoogle Scholar |

Chen H-M, Chang S-C, Wu C-C, Cuo T-S, Wu J-S, Juang R-H (2002) Regulation of the catalytic behaviour of L-form starch phosphorylase from sweet potato roots by proteolysis. Physiologia Plantarum 114, 506–515.
Regulation of the catalytic behaviour of L-form starch phosphorylase from sweet potato roots by proteolysis.Crossref | GoogleScholarGoogle Scholar | 11975723PubMed |

Choi Y, Sims GE, Murphy S, Miller JR, Chan AP (2012) Predicting the functional effect of amino acid substitutions and indels. PLoS One 7, e46688
Predicting the functional effect of amino acid substitutions and indels.Crossref | GoogleScholarGoogle Scholar | 23236387PubMed |

Cuesta-Seijo JA, Ruzanski C, Krucewicz K, Meier S, Hägglund P, Svensson B, Palcic MM (2017) Functional and structural characterization of plastidic starch phosphorylase during barley endosperm development. PLoS One 12, e0175488
Functional and structural characterization of plastidic starch phosphorylase during barley endosperm development.Crossref | GoogleScholarGoogle Scholar | 28407006PubMed |

da Mota RV, Cordenunsi BR, Do Nascimento JR, Purgatto E, Rosseto MR, Lajolo FM (2002) Activity and expression of banana starch phosphorylases during fruit development and ripening. Planta 216, 325–333.
Activity and expression of banana starch phosphorylases during fruit development and ripening.Crossref | GoogleScholarGoogle Scholar | 12447547PubMed |

Davies JN (1966) Occurrence of sucrose in the fruit species of Lycopersicon. Nature 209, 640–641.
Occurrence of sucrose in the fruit species of Lycopersicon.Crossref | GoogleScholarGoogle Scholar |

de Godoy A, Morita RJ, Gordenunsi BR, Lajolo FM, do Nascimento JRO (2009) Expression analysis of a set of genes related to the ripening of bananas and mangoes. Brazilian Journal of Plant Physiology 21, 251–259.
Expression analysis of a set of genes related to the ripening of bananas and mangoes.Crossref | GoogleScholarGoogle Scholar |

Dinar M, Stevens MA (1981) The relationship between starch accumulation and soluble solids content of tomato fruits. Journal of the American Society for Horticultural Science 106, 415–418.

Duwenig E, Steup M, Kossmann J (1997) Induction of genes encoding plastidic phosphorylase from spinach (Spinacia oleracea L.) and potato (Solanum tuberosum L.) by exogenously supplied carbohydrates in excised leaf discs. Planta 203, 111–120.

Egea I, Bian W, Barsan C, Jauneau A, Pech J-C, Latché A, Li Z, Chervin C (2011) Chloroplast to chromoplast transition in tomato fruit: spectral confocal microscopy analyses of carotenoids and chlorophylls in isolated plastids and time-lapse recording on intact live tissue. Annals of Botany 108, 291–297.
Chloroplast to chromoplast transition in tomato fruit: spectral confocal microscopy analyses of carotenoids and chlorophylls in isolated plastids and time-lapse recording on intact live tissue.Crossref | GoogleScholarGoogle Scholar | 21788376PubMed |

Elliott KJ, Butler WO, Dickinson CD, Konno Y, Vedvick TS, Fitzmaurice L, Mirkov TE (1993) Isolation and characterization of fruit vacuolar invertase genes from two tomato species and temporal differences in mRNA levels during fruit ripening. Plant Molecular Biology 21, 515–524.
Isolation and characterization of fruit vacuolar invertase genes from two tomato species and temporal differences in mRNA levels during fruit ripening.Crossref | GoogleScholarGoogle Scholar | 8095164PubMed |

Expósito-Rodríguez M, Borges A, Borges-Pérez A, Pérez A (2008) Selection of internal control genes for quantitative real-time RT-PCR studies during tomato development process. BMC Plant Biology 8, 131
Selection of internal control genes for quantitative real-time RT-PCR studies during tomato development process.Crossref | GoogleScholarGoogle Scholar | 19102748PubMed |

Fettke J, Hejazi M, Smirnova J, Hochel E, Stage M, Steup M (2009) Eukaryotic starch degradation: integration of plastidial and cytosolic pathways. Journal of Experimental Botany 60, 2907–2922.
Eukaryotic starch degradation: integration of plastidial and cytosolic pathways.Crossref | GoogleScholarGoogle Scholar | 19325165PubMed |

Fettke J, Leifels L, Brust H, Herbst K, Steup M (2012) Two carbon fluxes to reserve starch in potato (Solanum tuberosum L.) tuber cells are closely interconnected but differently modulated by temperature. Journal of Experimental Botany 63, 3011–3029.
Two carbon fluxes to reserve starch in potato (Solanum tuberosum L.) tuber cells are closely interconnected but differently modulated by temperature.Crossref | GoogleScholarGoogle Scholar | 22378944PubMed |

Gramzow L, Theißen G (2015) Phylogenomics reveals surprising sets of essential and dispensable clades of MIKC(c)-group MADS-box genes in flowering plants. Journal of Experimental Zoology. Part B, Molecular and Developmental Evolution 324, 353–362.
Phylogenomics reveals surprising sets of essential and dispensable clades of MIKC(c)-group MADS-box genes in flowering plants.Crossref | GoogleScholarGoogle Scholar | 25678468PubMed |

Guex N, Peitsch MC, Schwede T (2009) Automated comparative protein structure modeling with SWISS-MODEL and Swiss-PdbViewer: a historical perspective. Electrophoresis 30, S162–S173.
Automated comparative protein structure modeling with SWISS-MODEL and Swiss-PdbViewer: a historical perspective.Crossref | GoogleScholarGoogle Scholar | 19517507PubMed |

Hetherington S, Smillie R, Davies W (1998) Photosynthetic activities of vegetative and fruiting tissues of tomato. Journal of Experimental Botany 49, 1173–1181.
Photosynthetic activities of vegetative and fruiting tissues of tomato.Crossref | GoogleScholarGoogle Scholar |

Higgins JE, Kosar-Hashemi B, Li Z, Howitt CA, Larroque O, Flanagan B, Morell MK, Rahman S (2013) Characterization of starch phosphorylases in barley grains. Journal of the Science of Food and Agriculture 93, 2137–2145.
Characterization of starch phosphorylases in barley grains.Crossref | GoogleScholarGoogle Scholar | 23288583PubMed |

Ho LC, Hewitt JD (1986) Fruit development. In ‘The tomato crop’. (Ed. JG Atherton) pp. 201–240. (Chapman & Hall: New York)

Ho LC, Sjut V, Hoad GV (1983) The effect of assimilate supply of fruit growth and hormone levels in tomato plants. Plant Growth Regulation 1, 155–171.

Hsu JH, Yang CC, Su JC, Lee PD (2004) Purification and characterization of a cytosolic starch phosphorylase from etiolated rice seedlings. Botanical Bulletin of Academia Sinica 45, 187–196.

Hu T, Banzhaf W (2008) Nonsynonymous to synonymous substitution ratio ka/ks: measurement for rate of evolution in evolutionary computation. Lecture Notes in Computer Science 5199, 448–457.
Nonsynonymous to synonymous substitution ratio ka/ks: measurement for rate of evolution in evolutionary computation.Crossref | GoogleScholarGoogle Scholar |

Igic B, Lande R, Kohn JR (2008) Loss of self-incompatibility and its evolutionary consequences. International Journal of Plant Sciences 169, 93–104.
Loss of self-incompatibility and its evolutionary consequences.Crossref | GoogleScholarGoogle Scholar |

Kelley LA, Mezulis S, Yates CM, Wass MN, Sternberg MJ (2015) The Phyre2 web portal for protein modeling, prediction and analysis. Nature Protocols 10, 845–858.
The Phyre2 web portal for protein modeling, prediction and analysis.Crossref | GoogleScholarGoogle Scholar | 25950237PubMed |

Kortstee AJ, Appeldoorn NJ, Oortwijn ME, Visser RG (2007) Differences in regulation of carbohydrate metabolism during early fruit development between domesticated tomato and two wild relatives. Planta 226, 929–939.
Differences in regulation of carbohydrate metabolism during early fruit development between domesticated tomato and two wild relatives.Crossref | GoogleScholarGoogle Scholar | 17516079PubMed |

Kozlowski LP (2016) IPC – isoelectric point calculator. Biology Direct 11, 55
IPC – isoelectric point calculator.Crossref | GoogleScholarGoogle Scholar | 27769290PubMed |

Kumar A (1989) Starch phosphorylase in plants. Journal of Scientific and Industrial Research (New Delhi, India) 48, 568–576.

Kumar A, Sanwal GG (1977) Multiple forms of starch phosphorylase from banana leaves. Phytochemistry 16, 327–328.
Multiple forms of starch phosphorylase from banana leaves.Crossref | GoogleScholarGoogle Scholar |

Kumar A, Sanwal GG (1982) Purification and physicochemical properties of starch phosphorylase from young banana leaves. Biochemistry 21, 4152–4159.
Purification and physicochemical properties of starch phosphorylase from young banana leaves.Crossref | GoogleScholarGoogle Scholar | 7126533PubMed |

Ladizinsky G (1998) ‘Plant evolution under domestication.’ (Kluwer Academic Press: Dordrecht, The Netherlands)

Li L, Paulo MJ, Strahwald J, Lübeck J, Hofferbert HR, Tacke E, Junghans H, Wunder J, Draffehn A, van Eeuwijk F, Gebhardt C (2008) Natural DNA variation at candidate loci is associated with potato chip color, tuber starch content, yield and starch yield. Theoretical and Applied Genetics 116, 1167–1181.
Natural DNA variation at candidate loci is associated with potato chip color, tuber starch content, yield and starch yield.Crossref | GoogleScholarGoogle Scholar | 18379755PubMed |

Lira BS, Gramegna G, Trench BA, Alves FRR, Silva EM, Silva GFF, Thirumalaikumar VP, Lupi ACD, Demarco D, Purgatto E, Nogueira FTS, Balazadeh S, Freschi L, Rossi M (2017) Manipulation of a senescence-associated gene improves fleshy fruit yield. Plant Physiology 175, 77–91.
Manipulation of a senescence-associated gene improves fleshy fruit yield.Crossref | GoogleScholarGoogle Scholar | 28710129PubMed |

Luengwilai K, Tananuwong K, Shoemaker CF, Beckles DM (2010) Starch molecular structure shows little association with fruit physiology and starch metabolism in tomato. Journal of Agricultural and Food Chemistry 58, 1275–1282.
Starch molecular structure shows little association with fruit physiology and starch metabolism in tomato.Crossref | GoogleScholarGoogle Scholar | 20038101PubMed |

Marshall JA, Knapp S, Davey MR, Power JB, Cocking EC, Bennett MD, Cox AV (2001) Molecular systematics of Solanum section Lycopersicum (Lycopersicon) using the nuclear ITS rDNA region. Theoretical and Applied Genetics 103, 1216–1222.
Molecular systematics of Solanum section Lycopersicum (Lycopersicon) using the nuclear ITS rDNA region.Crossref | GoogleScholarGoogle Scholar |

Miller JS, Kostyun JL (2011) Functional gametophytic self-incompatibility in a peripheral population of Solanum peruvianum (Solanaceae). Heredity 107, 30–39.
Functional gametophytic self-incompatibility in a peripheral population of Solanum peruvianum (Solanaceae).Crossref | GoogleScholarGoogle Scholar | 21119705PubMed |

Mori H, Tanizawa K, Fukui T (1993) A chimeric alpha-glucan phosphorylase of plant type L and H isozymes. Functional role of 78-residue insertion in type L isozyme. Journal of Biological Chemistry 268, 5574–5581.

Nakano K, Fukui T (1986) The complete amino acid sequence of potato α-glucan phosphorylase. Journal of Biological Chemistry 261, 8230–8236.

Nakano K, Mori H, Fukui T (1989) Molecular cloning of cDNA encoding potato amyloplast α-glucan phosphorylase and the structure of its transit peptide. Journal of Biochemistry 106, 691–695.
Molecular cloning of cDNA encoding potato amyloplast α-glucan phosphorylase and the structure of its transit peptide.Crossref | GoogleScholarGoogle Scholar | 2481677PubMed |

Newgard CB, Hwang PK, Fletterick RJ (1989) The family of glycogen phosphorylases: structure and function. Critical Reviews in Biochemistry and Molecular Biology 24, 69–99.
The family of glycogen phosphorylases: structure and function.Crossref | GoogleScholarGoogle Scholar | 2667896PubMed |

Nighojkar SA, Kumar A (1997) Starch phosphorylase: biochemical, molecular and biotechnological aspects. Genetic Engineer and Biotechnologist 17, 189–202.

O’Neill EC, Rashid AM, Stevenson CEM, Hetru AC, Gunning AP, Rejzek M, Nepogodiev SA, Bornemann S, Lawson DM, Field RA (2014) Sugar-coated sensor chip and nanoparticle surfaces for the in vitro enzymatic synthesis of starch-like materials. Chemical Science 5, 341
Sugar-coated sensor chip and nanoparticle surfaces for the in vitro enzymatic synthesis of starch-like materials.Crossref | GoogleScholarGoogle Scholar |

Obiadalla-Ali H, Fernie AR, Kossmann J, Lloyd JR (2004) Developmental analysis of carbohydrate metabolism in tomato (Lycopersicon esculentum cv. Micro-Tom) fruits. Physiologia Plantarum 120, 196–204.
Developmental analysis of carbohydrate metabolism in tomato (Lycopersicon esculentum cv. Micro-Tom) fruits.Crossref | GoogleScholarGoogle Scholar | 15032853PubMed |

Orawetz T, Malinova I, Orzechowski S, Fettke J (2016) Reduction of the plastidic phosphorylase in potato (Solanum tuberosum L.) reveals impact on storage starch structure during growth at low temperature. Plant Physiology and Biochemistry 100, 141–149.
Reduction of the plastidic phosphorylase in potato (Solanum tuberosum L.) reveals impact on storage starch structure during growth at low temperature.Crossref | GoogleScholarGoogle Scholar | 26828405PubMed |

Pease JB, Haak DC, Hahn MW, Moyle LC (2016) Phylogenomics reveals three sources of adaptive variation during a rapid radiation. PLoS Biology 14, e1002379
Phylogenomics reveals three sources of adaptive variation during a rapid radiation.Crossref | GoogleScholarGoogle Scholar | 26871574PubMed |

Peralta IE, Spooner DM (2001) Granule-bound starch synthase (GBSSI) gene phylogeny of wild tomatoes (Solanum L. section Lycopersicon [Mill.] Wettst. subsection Lycopersicon). American Journal of Botany 88, 1888–1902.
Granule-bound starch synthase (GBSSI) gene phylogeny of wild tomatoes (Solanum L. section Lycopersicon [Mill.] Wettst. subsection Lycopersicon).Crossref | GoogleScholarGoogle Scholar | 21669622PubMed |

Peralta IE, Spooner DM, Knapp S (2008) Taxonomy of wild tomatoes and their relatives (Solanum sect. Lycopersicoides, sect. Juglandifolia, sect. Lycopersicon; Solanaceae. Systematic Botany Monographs 84, 1–186.

Proels RK, Hückelhoven R (2014) Cell-wall invertases, key enzymes in the modulation of plant metabolism during defense responses. Molecular Plant Pathology 15, 858–864.
Cell-wall invertases, key enzymes in the modulation of plant metabolism during defense responses.Crossref | GoogleScholarGoogle Scholar | 24646208PubMed |

Robinson NL, Hewitt JD, Bennett AB (1988) Sink metabolism in tomato fruit: I. Developmental changes in carbohydrate metabolizing enzymes. Plant Physiology 87, 727–730.
Sink metabolism in tomato fruit: I. Developmental changes in carbohydrate metabolizing enzymes.Crossref | GoogleScholarGoogle Scholar | 16666215PubMed |

Roth C, Liberles DA (2006) A systematic search for positive selection in higher plants (Embryophytes). BMC Plant Biology 6, 12
A systematic search for positive selection in higher plants (Embryophytes).Crossref | GoogleScholarGoogle Scholar | 16784532PubMed |

Satoh H, Shibahara K, Tokunaga T, Nishi A, Tasaki M, Hwang SK, Okita TW, Kaneko N, Fujita N, Yoshida M, Hosaka Y, Sato A, Utsumi Y, Ohdan T, Nakamura Y (2008) Mutation of the plastidic alpha-glucan phosphorylase gene in rice affects the synthesis and structure of starch in the endosperm. The Plant Cell 20, 1833–1849.
Mutation of the plastidic alpha-glucan phosphorylase gene in rice affects the synthesis and structure of starch in the endosperm.Crossref | GoogleScholarGoogle Scholar | 18621947PubMed |

Schaffer AA, Petreikov M (1997) Sucrose-to-starch metabolism in tomato fruit undergoing transient starch accumulation. Plant Physiology 113, 739–746.
Sucrose-to-starch metabolism in tomato fruit undergoing transient starch accumulation.Crossref | GoogleScholarGoogle Scholar | 12223639PubMed |

Schreiber L, Nader-Nieto AC, Schönhals EM, Walkemeier B, Gebhardt C (2014) SNPs in genes functional in starch-sugar interconversion associate with natural variation of tuber starch and sugar content of potato (Solanum tuberosum L.). G3 4, 1797–1811.
SNPs in genes functional in starch-sugar interconversion associate with natural variation of tuber starch and sugar content of potato (Solanum tuberosum L.).Crossref | GoogleScholarGoogle Scholar | 25081979PubMed |

Schupp N, Ziegler P (2004) The relation of starch phosphorylases to starch metabolism in wheat. Plant & Cell Physiology 45, 1471–1484.
The relation of starch phosphorylases to starch metabolism in wheat.Crossref | GoogleScholarGoogle Scholar |

Shima Y, Fujisawa M, Kitagawa M, Nakano T, Kimbara J, Nakamura N, Shiina T, Sugiyama J, Nakamura T, Kasumi T, Ito Y (2014) Tomato FRUITFULL homologs regulate fruit ripening via ethylene biosynthesis. Bioscience, Biotechnology, and Biochemistry 78, 231–237.
Tomato FRUITFULL homologs regulate fruit ripening via ethylene biosynthesis.Crossref | GoogleScholarGoogle Scholar | 25036675PubMed |

Slugina MA, Shchennikova AV, Kochieva EZ (2017) TAI vacuolar invertase orthologs: the interspecific variability in tomato plants (Solanum section Lycopersicon). Molecular Genetics and Genomics 292, 1123–1138.
TAI vacuolar invertase orthologs: the interspecific variability in tomato plants (Solanum section Lycopersicon).Crossref | GoogleScholarGoogle Scholar | 28634826PubMed |

Slugina MA, Shchennikova AV, Kochieva EZ (2018) LIN7 cell-wall invertase orthologs in cultivated and wild tomatoes (Solanum Section Lycopersicon). Plant Mol Biol Rep 36, 195–209.
LIN7 cell-wall invertase orthologs in cultivated and wild tomatoes (Solanum Section Lycopersicon).Crossref | GoogleScholarGoogle Scholar |

Sonnewald U, Basner A, Greve B, Steup M (1995) A second L-type isozyme of potato glucan phosphorylase: cloning, antisense inhibition and expression analysis. Plant Molecular Biology 27, 567–576.
A second L-type isozyme of potato glucan phosphorylase: cloning, antisense inhibition and expression analysis.Crossref | GoogleScholarGoogle Scholar | 7894019PubMed |

St-Pierre B, Bertrand C, Camirand A, Cappadocia M, Brisson N (1996) The starch phosphorylase gene is subjected to different modes of regulation in starch-containing tissues of potato. Plant Molecular Biology 30, 1087–1098.
The starch phosphorylase gene is subjected to different modes of regulation in starch-containing tissues of potato.Crossref | GoogleScholarGoogle Scholar | 8704121PubMed |

Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.
MEGA6: Molecular Evolutionary Genetics Analysis version 6.0.Crossref | GoogleScholarGoogle Scholar | 24132122PubMed |

Tanksley SD (2004) The genetic, developmental, and molecular bases of fruit size and shape variation in tomato. The Plant Cell 16, S181–S189.
The genetic, developmental, and molecular bases of fruit size and shape variation in tomato.Crossref | GoogleScholarGoogle Scholar | 15131251PubMed |

Thanou M, Tsaniklidis G, Delis C, Nikolopoulou A-E, Nikoloudakis N, Karapanos I, Aivalakis G (2016) Gene transcript accumulation and enzyme activity of β-amylases suggest involvement in the starch depletion during the ripening of cherry tomatoes Plant Gene 5, 8–12.
Gene transcript accumulation and enzyme activity of β-amylases suggest involvement in the starch depletion during the ripening of cherry tomatoesCrossref | GoogleScholarGoogle Scholar |

The 100 Tomato Genome Sequencing Consortium et al. (2014) Exploring genetic variation in the tomato (Solanum section Lycopersicon) clade by whole-genome sequencing. The Plant Journal 80, 136–148.
Exploring genetic variation in the tomato (Solanum section Lycopersicon) clade by whole-genome sequencing.Crossref | GoogleScholarGoogle Scholar | 25039268PubMed |

Tickle P, Burrell MM, Coates SA, Emes MJ, Tetlow IJ, Bowsher CG (2009) Characterization of plastidic starch phosphorylase in Triticum aestivum L. endosperm. Journal of Plant Physiology 166, 1465–1478.
Characterization of plastidic starch phosphorylase in Triticum aestivum L. endosperm.Crossref | GoogleScholarGoogle Scholar | 19524321PubMed |

Vallarino JG, Yeats TH, Maximova E, Rose JK, Fernie AR, Osorio S (2017) Postharvest changes in LIN5-down-regulated plants suggest a role for sugar deficiency in cuticle metabolism during ripening. Phytochemistry 142, 11–20.
Postharvest changes in LIN5-down-regulated plants suggest a role for sugar deficiency in cuticle metabolism during ripening.Crossref | GoogleScholarGoogle Scholar | 28658609PubMed |

Waters MT, Langdale JA (2009) The making of a chloroplast. EMBO Journal 28, 2861–2873.
The making of a chloroplast.Crossref | GoogleScholarGoogle Scholar | 19745808PubMed |

Yelle S, Hewitt JD, Robinson NL, Damon S, Bennett AB (1988) Sink metabolism in tomato fruit: III. Analysis of carbohydrate assimilation in a wild species. Plant Physiology 87, 737–740.
Sink metabolism in tomato fruit: III. Analysis of carbohydrate assimilation in a wild species.Crossref | GoogleScholarGoogle Scholar | 16666217PubMed |

You C, Chen H, Myung S, Sathitsuksanoh N, Ma H, Zhang XZ, Li J, Zhang YH (2013) Enzymatic transformation of nonfood biomass to starch. Proceedings of the National Academy of Sciences of the United States of America 110, 7182–7187.
Enzymatic transformation of nonfood biomass to starch.Crossref | GoogleScholarGoogle Scholar | 23589840PubMed |

Yu Y, Mu HH, Wasserman BP, Carman GM (2001) Identifcation of the maize amyloplast stromal 112-kD protein as a plastidic starch phosphorylase. Plant Physiology 125, 351–359.
Identifcation of the maize amyloplast stromal 112-kD protein as a plastidic starch phosphorylase.Crossref | GoogleScholarGoogle Scholar | 11154342PubMed |

Zeeman SC, Thorneycroft D, Schupp N, Chapple A, Weck M, Dunstan H, Haldimann P, Bechtold N, Smith AM, Smith SM (2004) The role of plastidial α-glucan phosphorylase in starch degradation and tolerance of abiotic stress in Arabidopsis leaves. Plant Physiology 135, 849–858.
The role of plastidial α-glucan phosphorylase in starch degradation and tolerance of abiotic stress in Arabidopsis leaves.Crossref | GoogleScholarGoogle Scholar | 15173560PubMed |

Zeeman SC, Kossmann J, Smith AM (2010) Starch: its metabolism, evolution, and biotechnological modification in plants. Annual Review of Plant Biology 61, 209–234.
Starch: its metabolism, evolution, and biotechnological modification in plants.Crossref | GoogleScholarGoogle Scholar | 20192737PubMed |

Zuriaga E, Blanca J, Nuez F (2009) Classification and phylogenetic relationships in Solanum section Lycopersicon based on AFLP and two nuclear gene sequences. Genetic Resources and Crop Evolution 56, 663–678.
Classification and phylogenetic relationships in Solanum section Lycopersicon based on AFLP and two nuclear gene sequences.Crossref | GoogleScholarGoogle Scholar |