Abstract
Key message
Comparative ultrastructural developmental time-course analysis has identified discrete stages at which the fruit plastids undergo structural and consequently functional transitions to facilitate subsequent development-guided understanding of the complex plastid biology.
Abstract
Plastids are the defining organelle for a plant cell and are critical for myriad metabolic functions. The role of leaf plastid, chloroplast, is extensively documented; however, fruit plastids—chromoplasts—are poorly understood, especially in the context of the diverse metabolic processes operating in these diverse plant organs. Recently, in a comparative study of the predicted plastid-targeted proteomes across seven plant species, we reported that each plant species is predicted to harbor a unique set of plastid-targeted proteins. However, the temporal and developmental context of these processes remains unknown. In this study, an ultrastructural analysis approach was used to characterize fruit plastids in the epidermal and collenchymal cell layers at 11 developmental timepoints in three genotypes of apple (Malus × domestica Borkh.): chlorophyll-predominant ‘Granny Smith’, carotenoid-predominant ‘Golden Delicious’, and anthocyanin-predominant ‘Top Red Delicious’. Plastids transitioned from a proplastid-like plastid to a chromoplast-like plastid in epidermis cells, while in the collenchyma cells, they transitioned from a chloroplast-like plastid to a chloro-chromo-amyloplast plastid. Plastids in the collenchyma cells of the three genotypes demonstrated a diverse array of structures and features. This study enabled the identification of discrete developmental stages during which specific functions are most likely being performed by the plastids as indicated by accumulation of plastoglobuli, starch granules, and other sub-organeller structures. Information regarding the metabolically active developmental stages is expected to facilitate biologically relevant omics studies to unravel the complex biochemistry of plastids in perennial non-model systems.
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References
Abramoff M, Magalhaes P, Ram S (2004) Image processing with ImageJ. Biophoton Int 11:36–42
Alexander L, Grierson D (2002) Ethylene biosynthesis and action in tomato: a model for climacteric fruit ripening. J Exp Bot 53:2039–2055
Barsan C, Sanchez-Bel P, Rombaldi C, Egea I, Rossignol M, Kuntz M, Zouine M, Latche A, Bouzayen M, Pech JC (2010) Characteristics of the tomato chromoplast revealed by proteomic analysis. J Exp Bot 61:2413–2431
Bartley IM, Stoker PG, Martin ADE, Hatfield SGS, Knee M (1985) Synthesis of aroma compounds by apples supplied with alcohols and methyl-esters of fatty-acids. J Sci Food Agric 36:567–574
Bizjak J, Mikulic-Petkovsek M, Stampar F, Veberic R (2013) Changes in primary metabolites and polyphenols in the peel of “Braeburn” apples (Malus domestica Borkh.) during advanced maturation. J Agric Food Chem 61:10283–10292
Blanke MM, Notton BA, Hucklesby DP (1986) Physical and kinetic-properties of photosynthetic phosphoenolpyruvate carboxylase in developing apple fruit. Phytochemistry 25:601–606
Bonora A, Pancaldi S, Gualandri R, Fasulo MP (2000) Carotenoid and ultrastructure variations in plastids of Arum italicum Miller fruit during maturation and ripening. J Exp Bot 51:873–884
Bouvier F, Camara B (2006) The role of plastids in ripening fruits. In: Wise RR, Hoober JK (eds) Advances in photosynthesis and respiration. Springer, Dordrecht, pp 419–432
Brookfield P, Murphy P, Harker R, MacRae E (1997) Starch degradation and starch pattern indices; Interpretation and relationship to maturity. Postharvest Biol Technol 11:23–30
Bulens I, Van de Poel B, Hertog M, Cristescu SM, Harren FJM, De Proft MP, Geeraerd AH, Nicolai BM (2014) Dynamic changes of the ethylene biosynthesis in ‘Jonagold’ apple. Physiol Plant 150:161–173
Camara B, Hugueney P, Bouvier F, Kuntz M, Moneger R (1995) Biochemistry and molecular biology of chromoplast development. Int Rev Cytol 163(163):175–247
Cheung AY, McNellis T, Piekos B (1993) Maintenance of chloroplast components during chromoplast differentiation in the tomato mutant green flesh. Plant Physiol 101:1223–1229
Clijsters H (1969) On the photosynthetic activity of developing apple fruits. Qualitas Plantarum et Materiae Vegetabiles 19:129–140
Cookson PJ, Kiano JW, Shipton CA, Fraser PD, Romer S, Schuch W, Bramley PM, Pyke KA (2003) Increases in cell elongation, plastid compartment size and phytoene synthase activity underlie the phenotype of the high pigment-1 mutant of tomato. Planta 217:896–903
Cornah JE, Roper JM, Singh DP, Smith AG (2002) Measurement of ferrochelatase activity using a novel assay suggests that plastids are the major site of haem biosynthesis in both photosynthetic and non-photosynthetic cells of pea (Pisum sativum L.). Biochem J 362:423–432
Echeverria G, Graell J, Lopez ML, Lara I (2004) Volatile production, quality and aroma-related enzyme activities during maturation of ‘Fuji’ apples. Postharvest Biol Technol 31:217–227
Egea I, Barsan C, Bian W, Purgatto E, Latche A, Chervin C, Bouzayen M, Pech J-C (2010) Chromoplast differentiation: current status and perspectives. Plant Cell Physiol 51:1601–1611
Fischer K, Weber A (2002) Transport of carbon in non-green plastids. Trends Plant Sci 7:345–351
Fu XM, Kong WB, Peng G, Zhou JY, Azam M, Xu CJ, Grierson D, Chen KS (2012) Plastid structure and carotenogenic gene expression in red- and white-fleshed loquat (Eriobotrya japonica) fruits. J Exp Bot 63:341–354
Herrmann KM, Weaver LM (1999) The shikimate pathway. Annu Rev Plant Physiol Plant Mol Biol 50:473–503
Huff A (1983) Nutritional control of regreening and degreening in citrus peel segments. Plant Physiol 73:243–249
Huff A (1984) Sugar regulation of plastid interconversions in epicarp of citrus-fruit. Plant Physiol 76:307–312
Jackson JE (2003) Fruit skin color, russet and cracking. Biology of apples and pears. Cambridge University Press, Cambridge, pp 317–324
Janssen BJ, Thodey K, Schaffer RJ, Alba R, Balakrishnan L, Bishop R, Bowen JH, Crowhurst RN, Gleave AP, Ledger S, McArtney S, Pichler FB, Snowden KC, Ward S (2008) Global gene expression analysis of apple fruit development from the floral bud to ripe fruit. BMC Plant Biol 8:16
Knee M (1972) Anthocyanin, carotenoid, and chlorophyll changes in the peel of Cox’s Orange Pippin apples during ripening on and off the tree. J Exp Bot 23:184–196
Knee M (1988) Carotenol esters in developing apple fruits. Phytochemistry 27:1005–1009
Kovacs E, Eads TM (1999) Morphologic changes of starch granules in the apple cv. Mutsu during ripening and storage. Scanning 21:326–333
Kreuz K, Kleinig H (1984) Synthesis of prenyllipids in cells of spinach leaf. Compartmentation of enzymes for formation of isopentenyl diphosphate. Eur J Biochem 141:531–535
Lara I, Mio RM, Fuentes T, Sayez G, Graell J, Lopez ML (2003) Biosynthesis of volatile aroma compounds in pear fruit stored under long-term controlled-atmosphere conditions. Postharvest Biol Technol 29:29–39
Laval-Martin D (1974) Maturation of the cherry tomato fruit: evidence, by freeze-etched studies, of the evolution of chloroplasts in two classes of chromoplasts (author’s transl). Protoplasma 82:33–59
Liu Y, Roof S, Ye Z, Barry C, van Tuinen A, Vrebalov J, Bowler C, Giovannoni J (2004) Manipulation of light signal transduction as a means of modifying fruit nutritional quality in tomato. Proc Natl Acad Sci USA 101:9897–9902
Maloney GS, Kochevenko A, Tieman DM, Tohge T, Krieger U, Zamir D, Taylor MG, Fernie AR, Klee HJ (2010) Characterization of the branched-chain amino acid aminotransferase enzyme family in tomato. Plant Physiol 153:925–936
Martini M, Figueira A, Lenci C, Tavares D (2008) Polyphenolic cells and their interrelation with cotyledon cells in seven species of Theobroma (Sterculiaceae). Braz J Bot 31:425–431
Matile P (2000) Biochemistry of Indian summer: physiology of autumnal leaf coloration. Exp Gerontol 35:145–158
Mayfield SP, Huff A (1986) Accumulation of chlorophyll, chloroplastic proteins, and thylakoid membranes during reversion of chromoplasts to chloroplasts in citrus-sinensis epicarp. Plant Physiol 81:30–35
Merzlyak MN, Chivkunova OB (2000) Light-stress-induced pigment changes and evidence for anthocyanin photoprotection in apples. J Photochem Photobiol B 55:155–163
Merzlyak MN, Solovchenko AE (2002) Photostability of pigments in ripening apple fruit: a possible photoprotective role of carotenoids during plant senescence. Plant Sci 163:881–888
Mettal U, Boland W, Beyer P, Kleinig H (1988) Biosynthesis of monoterpene hydrocarbons by isolated chromoplasts from daffodil flowers. Eur J Biochem 170:881–888
Montefiori M, McGhie TK, Hallett IC, Costa G (2009) Changes in pigments and plastid ultrastructure during ripening of green-fleshed and yellow-fleshed kiwifruit. Sci Hortic 119:377–387
Murata M, Tsurutani M, Hagiwara S, Homma S (1997) Subcellular location of polyphenol oxidase in apples. Biosci Biotechnol Biochem 61:1495–1499
Nacir H, Brehelin C (2013) When proteomics reveals unsuspected roles: the plastoglobule example. Front Plant Sci 4:114
Phan CT (1973) Chloroplasts of the peel and the internal tissues of apple-fruits. Experientia 29:1555–1557
Phan CT (1984) All-granal chloroplasts of apple fruit. In: Sybesma C (ed) Advances in photosynthesis research research. Martinus Nijhoff/Dr. W. Junk Publishers, The Hague, pp 63–66
Rawsthorne S (2002) Carbon flux and fatty acid synthesis in plants. Prog Lipid Res 41:182–196
Reid M, Padfiels C, Watkins P, Harman J (1982) Starch iodine pattern as a maturity index for Granny Smith apples. N Z J Agric Res 25:229–273
Rowan DD, Lane HP, Allen JM, Fielder S, Hunt MB (1996) Biosynthesis of 2-methylbutyl, 2-methyl-2-butenyl and 2-methylbutanoate esters in Red Delicious and Granny Smith apples using deuterium-labeled substrates. J Agric Food Chem 44:3276–3285
Sanz C, Olias JM, Perez AG (1996) Aroma biochemistry of fruits and vegetables. In: Proceedings of the Phytochemical Society of Europe. Oxford University Press Inc., Oxford, pp 125–156
Schaeffer S, Harper A, Raja R, Jaiswal P, Dhingra A (2014) Comparative analysis of predicted plastid-targeted proteomes of sequenced higher plant genomes. PLoS One 9:e112870
Simpson DJ, Baqar M, Lee T (1975) Unusual ultrastructural features of the chloroplast-chromoplast transformation in Solanum luteum fruit. Aust J Plant Physiol 2:235–245
Sivak M (1998) Biochemistry, molecular biology and regulation of starch synthesis. Genet Eng Princ Methods 20:177–223
Skene DS (1962) Fruit skin structure in some tree fruits with special reference to russeting of apples, Ph.D. thesis. University of London, London
Vidi PA, Kanwischer M, Baginsky S, Austin JR, Csucs G, Dormann P, Kessler F, Brehelin C (2006) Tocopherol cyclase (VTE1) localization and vitamin E accumulation in chloroplast plastoglobule lipoprotein particles. J Biol Chem 281:11225–11234
Waters MT, Fray RG, Pyke KA (2004) Stromule formation is dependent upon plastid size, plastid differentiation status and the density of plastids within the cell. Plant J 39:655–667
Webb DT (1982) Structure and ultrastructure of plastids in Light-Grown and Dark-Grown Zamia-Floridana Dc—seedling roots invitro. New Phytol 91:721–725
Ytterberg AJ, Peltier JB, van Wijk KJ (2006) Protein profiling of plastoglobules in chloroplasts and chromoplasts. A surprising site for differential accumulation of metabolic enzymes. Plant Physiol 140:984–997
Acknowledgements
The authors thank Deb Pehrson for assistance with sample procurement at Washington State University Tukey Orchard and Chris Davitt for assistance with sample fixation. This work was supported in part by WSU Startup and ARC Hatch Funds to AD. NCV acknowledges the McNair Fellowship program and RC acknowledges the WSU CAHNRS undergraduate research fellowship and Auvil Fellowship for undergraduate research experience. S.M.S. and R.C. acknowledge the support received from National Institutes of Health/National Institute of General Medical Sciences through an institutional training grant award T32-GM008336. Its contents are solely the responsibility of the authors and do not necessarily represent the official views of the NIGMS or NIH.
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Communicated by Prakash P. Kumar.
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Schaeffer, S.M., Christian, R., Castro-Velasquez, N. et al. Comparative ultrastructure of fruit plastids in three genetically diverse genotypes of apple (Malus × domestica Borkh.) during development. Plant Cell Rep 36, 1627–1640 (2017). https://doi.org/10.1007/s00299-017-2179-z
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DOI: https://doi.org/10.1007/s00299-017-2179-z