Ultrastructural Analyses of Senescence Associated Dismantling of Chloroplasts Revisited

  • Maria Mulisch
  • Karin KrupinskaEmail author
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 36)


During leaf senescence, chloroplasts are transformed into gerontoplasts involving typical structural changes that have been revealed by electron microscopy for more than 30 years. The structural changes involved in chloroplast-to-gerontoplast transition affect the organization of the thylakoid membrane system which is progressively degraded. In parallel, the number and size of plastoglobules was observed to increase. The internal changes in the structure of chloroplasts occurring during leaf senescence are accompanied by a change from an ellipsoid to a round shape and by a reduction in volume. Recent results on Rubisco degradation involving modern cell biology approaches suggest that plastids during senescence release material including Rubisco and other stromal proteins for degradation outside the organelle. In order to get further insight into the structural changes associated with chloroplast dismantling, we have revisited the pertinent literature and furthermore analyzed the ultrastructure of chloroplasts at different stages of barley leaf senescence and under different conditions leading to yellowing of the leaves. Specific changes at the periphery of chloroplasts at certain stages during aging might be related to an exchange of material between chloroplasts and the endoplasmic reticulum. Electron microscopy cannot, however, discriminate between anterograde and retrograde vesicle movements. Electron lucent areas in the matrix of chloroplasts indicate that protein degradation occurs not only outside but also inside the organelle.

In many studies it has been observed that the number of plastids per cell declines at late stages of senescence. Our ultrastructural analyses of leaves senescing under field conditions showed that chloroplasts as well as gerontoplasts are surrounded by membranous structures before they are engulfed by the vacuole. Thus, the autophagy pathway appears to be involved in senescence.

Many results of electron microscopical analyses of leaf senescence indicate that there exist several mechanisms of chloroplast dismantling. However, further studies by live-cell imaging, immunolabeling and cryo-electron microscopical methods on defined material of plants grown under strictly controlled and comparable conditions will be required for elucidating the mechanisms involved.


Thylakoid Membrane Leaf Senescence Flag Leave Barley Leave Central Vacuole 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


ATG genes –

Autophagy related genes;


Confocal laser scanning microscopy;




Electron microscopy;


Endoplasmic reticulum;


Green fluorescence protein;

h D

Hours in darkness;

h L

Hours in light;


Precursor protease vesicle(s);


Protein storage vesicle(s);


Rubisco-containing body(s);


Rubisco-containing vesicle(s);


Rough endoplasmic reticulum;


Ribulose-1,5-bisphosphate carboxylase oxygenase;


Senescence-associated vacuole;


Tonoplast intrinsic protein


  1. Anderson JM (1999) Insights into the consequence of grana stacking of thylakoid membranes in vascular plants: a personal perspective. Aust J Plant Physiol 26:625–639Google Scholar
  2. Anderson JM, Andersson B (1982) The architecture of photosynthetic membranes – lateral and transverse organization. Trends Biochem Sci 7:288–292Google Scholar
  3. Andersson MX, Goksor M, Sandelius AS (2007) Optical manipulation reveals strong attracting forces at membrane contact sites between endoplasmic reticulum and chloroplasts. J Biol Chem 282:1170–1174PubMedGoogle Scholar
  4. Andrade-Navarro MA, Sanchez-Pulido L, McBride HM (2009) Mitochondrial vesicles: an ancient process providing new links to peroxisomes. Curr Opin Cell Biol 21:560–567PubMedGoogle Scholar
  5. Austin J, Frost E, Vidi P-A, Kessler F, Staehelin L (2006) Plastoglobules are lipoprotein subcompartments of the chloroplast that are permanently coupled to thylakoid membranes and contain biosynthetic enzymes. Plant Cell 18:1693–1703PubMedGoogle Scholar
  6. Barton R (1966) Fine structure of mesophyll cells in senescing leaves of Phaseolus. Planta 71:314–325Google Scholar
  7. Bayer RG, Stael S, Csaszar E, Teige M (2011) Mining the soluble chloroplast proteome by affinity chromatography. Proteomics 11:1287–1299PubMedGoogle Scholar
  8. Benning C, Xu CC, Awai K (2006) Non-vesicular and vesicular lipid trafficking involving plastids. Curr Opin Plant Biol 9:241–247PubMedGoogle Scholar
  9. Biswal UC, Biswal B (1988) Ultrastructural modifications and biochemical changes during senescence of chloroplasts. Int Rev Cytol 113:271–321Google Scholar
  10. Biswal UC, Biswal B, Raval MK (2003) Chloroplast biogenesis: from proplastid to gerontoplast. Kluwer, DordrechtGoogle Scholar
  11. Butler RD (1967) The fine structure of senescing cotyledons of cucumber. J Exp Bot 18:535–543Google Scholar
  12. Camp PJ, Huber SC, Burke JJ, Moreland DE (1982) Biochemical changes that occur during senescence of wheat leaves. Plant Physiol 70:1641–1646PubMedGoogle Scholar
  13. Chiba A, Ishida H, Nishizawa NK, Makino A, Mae T (2003) Exclusion of ribulose 1,5-bisphosphate carboxylase/oxygenase from chloroplasts by specific bodies in naturally senescing leaves of wheat. Plant Cell Physiol 44:914–921PubMedGoogle Scholar
  14. Chonan N, Kawahara H, Matsuda T (1977) Changes in chloroplast ultrastructure during senescence of leaves in rice plants. Jap J Crop Sci 46:379–386Google Scholar
  15. Chrost B, Falk J, Kernebeck B, Mölleken H, Krupinska K (1999) Tocopherol biosynthesis in senescing chloroplasts – a mechanism to protect envelope membranes against oxidative stress and a prerequisite for lipid remobilization? In: Argyroudi-Akoyunoglou JH, Senger H (eds) The Chloroplast: from molecular biology to biotechnology. Kluwer, Dordrecht, pp 171–176Google Scholar
  16. Crotty WJ, Ledbetter MC (1973) Membrane continuities involving chloroplasts and other organelles in plant cells. Science 182:839–841PubMedGoogle Scholar
  17. Dertinger U, Schaz U, Schulze ED (2003) Age-dependence of the antioxidative system in tobacco with enhanced glutathione reductase activity or senescence-induced production of cytokinins. Physiol Plant 119:19–29Google Scholar
  18. Eilam Y, Butler RD, Simon EW (1971) Ribosomes and polysomes in cucumber leaves during growth and senescence. Plant Physiol 47:317–323PubMedGoogle Scholar
  19. Falk J, Andersen G, Kernebeck B, Krupinska K (2003) Constitutive overexpression of barley 4-hydroxyphenylpyruvate dioxygenase in tobacco results in elevation of the Vitamin E content in seeds but not in leaves. FEBS Lett 540:35–40PubMedGoogle Scholar
  20. Gärtner P-J, Nagl W (1980) Acid phosphatase activity in plastids (plastolysomes) of senescing embryo-suspensor cells. Planta 149:341–349Google Scholar
  21. Gepstein S (1988) Photosynthesis. In: Noodén LD, Leopold AC (eds) Senescence and aging in plants. Academic, San Diego, pp 85–111Google Scholar
  22. Ghosh S, Hudak K, Dumbroff EB, Thompson JE (1994) Release of photosynthetic catabolites by blebbing from thylakoids. Plant Physiol 106:1547–1553PubMedGoogle Scholar
  23. Ghosh S, Mahoney SR, Penterman JN, Peirson D, Dumbroff EB (2001) Ultrastructural and biochemical changes in chloroplasts during Brassica napus senescence. Plant Physiol Biochem 39:777–784Google Scholar
  24. Gibbs S (1981) The chloroplast endoplasmic reticulum: structure, function, and evolutionary significance. Int Rev Cytol 72:49–99Google Scholar
  25. Greenwood JS, Hem M, Gietl C (2005) Ricinosomes and endosperm transfer cell structure in programmed cell death of the nucellus during Ricinus seed deve­lopment. Proc Natl Acad Sci USA 102:2238–2243Google Scholar
  26. Guiamet JJ, Pichersky E, Nooden LD (1999) Mass exodus from senescing soybean chloroplasts. Plant Cell Physiol 40:986–992Google Scholar
  27. Gunning BES (2005) Plastid stromules: video microscopy of their outgrowth, retraction, tensioning, anchoring, bridging, and tip-shedding. Protoplasma 225:33–42PubMedGoogle Scholar
  28. Harris JB (1978) Development of a tubular apparatus in chloroplasts of aging Cyphomandra leaves. Cytobios 21:151–164PubMedGoogle Scholar
  29. Harris JB, Arnott HJ (1973) Effects of senescence on chloroplasts of tobacco leaf. Tissue Cell 5:527–544PubMedGoogle Scholar
  30. Harris JB, Schaefer VG (1981) Some correlated events in aging leaf tissue of tree tomato and tobacco. Botanica Gazetta 142:43–54Google Scholar
  31. Hashimoto H, Kura-Hotta M, Shirano Y, Kato T, Hayashi H, Shibata D, Tabata S, Ohsumi Y (1989) Changes in protein content and in structure and number of chloroplasts during leaf senescence in rice seedlings. Plant Physiol 30:707–777Google Scholar
  32. He P, Osaki M, Takebe M, Shinano T, Wasaki J (2005) Endogenous hormones and expression of senescence-related genes in different senescent types of maize. J Exp Bot 56:1117–1128PubMedGoogle Scholar
  33. Hernandez VJ, Schaedle M (1973) Functional and structural changes in senescing Populus deltoides (Batr.) chloroplasts. Plant Physiol 51:245–249Google Scholar
  34. Huber DJ, Newman DW (1976) Relationship between lipid changes and plastid ultrastructural changes in senescing and regreening soybean cotyledons. J Exp Bot 27:490–511Google Scholar
  35. Humbeck K, Quast S, Krupinska K (1996) Functional and molecular changes in the photosynthetic apparatus during senescence of flag leaves from field-grown barley plants. Plant Cell Environ 19:337–344Google Scholar
  36. Hurkman WJ (1979) Ultrastructural changes of chloroplasts in attached and detached, aging primary wheat leaves. Am J Bot 66:64–70Google Scholar
  37. Ishida H, Yoshimoto K, Izuni M, Reisen D, Yano Y, Makino A, Ohsumi Y, Hanson M, Mae T (2008) Mobilization of Rubisco and stroma-localized fluorescent proteins of chloroplasts to the vacuole by an ATG gene-dependent autophagic process. Plant Physiol 148:142–155PubMedGoogle Scholar
  38. Kolodziejek I, Koziol I, Waleza M, Mostowska A (2003) Ultrastructure of mesophyll cells and pigment content in senescing leaves of maize and barley. J Plant Growth Regul 22:217–227Google Scholar
  39. Kolodziejek I, Waleza M, Mostowska A (2006) Morphological, histochemical and ultrastructural indicators of maize and barley leaf senescence. Biol Plant 50:565–573Google Scholar
  40. Krupinska K (2006) Fate and activities of plastids during leaf senescence. In: Wise R, Hoober J (eds) The structure and function of plastids. Springer, Dordrecht, pp 433–449Google Scholar
  41. Krupinska K (2011) Plastiden und Zellkern im Zwiegespräch. BIUZ 41:298–305Google Scholar
  42. Krupinska K, Mulisch M, Hollmann J, Tokarzc K, Zschiesche W, Kage H, Humbeck K, Bilger W (2012) An alternative strategy of dismantling of the chloroplasts during leaf senescence observed in a high yield variety of barley. Physiol Plant 144:189–200PubMedGoogle Scholar
  43. Kunst L, Wrischer M (1984) Adaptational changes of plastids in the leaves of Ligustrum ovalifolium Hassk var aureum at different light intensities. Protoplasma 122:132–137Google Scholar
  44. Kura-Hotta M, Hashimoto H, Satoh K, Katoh S (1990) Quantitative determination of changes in the number and size of chloroplasts in naturally senescing leaves of rice seedlings. Plant Cell Physiol 31:33–38Google Scholar
  45. Kutik J (1998) The development of chloroplast structure during leaf ontogeny. Photosynthetica 35:481–505Google Scholar
  46. Lichtenthaler HK (1966) Verbreitung und Konzentration des a-Tocopherols in Chloroplasten. Ber Dtsch Bot Ges 79:111–117Google Scholar
  47. Lichtenthaler HK (1968) Plastoglobules and the fine structure of plastids. Endeavour 27:144–149Google Scholar
  48. Lichtenthaler HK (1969) Die Plastoglobuli von Spinat, ihre Größe und Zusammensetzung während der Chloroplastendegeneration. Protoplasma 68:315–326Google Scholar
  49. Lichtenthaler HK (1970) Die Lokalisation der Plastidenchinone in den Chromoplasten der Petalen von Sarothamnus scoparius (L) Wimm ex Koch. Planta 90:142–152Google Scholar
  50. Lichtenthaler HK, Sprey B (1966) Ultrastructural changes in chloroplasts of detached parsley leaves. Z Naturforsch 21b:690–697Google Scholar
  51. Lichtenthaler HK, Weinert H (1970) Die Beziehungen ­zwischen Lipochinonbiosynthese und Plastoglo­bulibildung in den Chloroplasten von Ficus elastica Roxb. Zeitschrift für Naturforschung 25b:619–623Google Scholar
  52. Ljubešić N (1968) Feinbau der Chloroplasten während der Vergilbung und Wiederergrünung der Blätter. Protoplasma 66:369–379Google Scholar
  53. Mae T, Kai N, Makino A, Ohira K (1984) Relation between ribulose bisphosphate carboxylase content and chloroplast number in naturally senescing primary leaves of wheat. Plant Cell Physiol 25:333–336Google Scholar
  54. Martínez DE, Costa ML, Guiamet JJ (2008) Senescence-associated degradation of chloroplast proteins inside and outside the organelle. Plant Biol 10:15–22PubMedGoogle Scholar
  55. Matile P (1975) The lytic compartment of plant cells. Cell Biology Monographs, vol. 1, Springer, BerlinGoogle Scholar
  56. Matile P (1992) Chloroplast senescence. In: Baker NR, Thomas H (eds) Crop photosynthesis: spatial and temporal determinants. Elsevier, Amsterdam, pp 423–440Google Scholar
  57. Matile P (1997) The vacuole and cell senescence. Adv Bot Res 25:87–112Google Scholar
  58. Minamikawa T, Toyooka K, Okamoto T, Hara-Nishimura I, Nishimura M (2001) Degradation of ribulose-bisphosphate carboxylase by vacuolar enzymes of senescing French bean leaves: immunocytochemical and ultrastructural observations. Protoplasma 218:144–153PubMedGoogle Scholar
  59. Mittelhäuser CJ, Van Stevenick RFM (1971) The ultrastructure of wheat leaves. 1. Changes due to natural senescence and the effects of kinetin and ABA on detached leaves incubated in the dark. Protoplasma 73:239–252Google Scholar
  60. Mlodzianowski F (1975) Ultrastrucutral changes in chloroplasts of Populis tremula L., leaves affected by the fungus Melampsora pinitorqua Braun. Rostr. Physiol Plant Pathol 6:1–3Google Scholar
  61. Mlodzianowski F, Mlozianowska L (1973) Chloroplast degeneration and its inhibition by kinetin in detached parsley leaves of Cichorium intybus L. Acta Soc Bot Pol XLII:649–656Google Scholar
  62. Mlodzianowski F, Ponitka A (1973) Ultrastructural changes of chloroplasts in detached parsley leaves yellowing in darkness and the influence of kinetin on that process. Z Pflanzenphysiol 69:13–25Google Scholar
  63. Mlodzianowski F, Siwecki R (1975) Ultrastructural changes in chloroplasts of Populus tremula L. Leaves affected by the fungus Melampsora pinitorqua Braun. Rostr Physiol Pl Pathol 6:1–3Google Scholar
  64. Morris K, Mackerness SA, Page T, John F, Murphy AM, Carr JP, Buchanan-Wollaston V (2000) Salicylic acid has a role in regulating gene expression during leaf senescence. Plant J 23:677–685PubMedGoogle Scholar
  65. Neuspiel M, Schauss AC, Braschi E, Zunino R, Rippstein P, Rachubinski RA, Andrade-Navarro MA, McBride HM (2008) Cargo-selected transport from the mitochondria to peroxisomes is mediated by vesicular carriers. Curr Biol 18:102–108PubMedGoogle Scholar
  66. Niewiadomska E, Polzien L, Desel C, Miszalski Z, Krupinska K (2009) Spatial patterns of senescence and development-dependent distribution of reactive oxygen species in tobacco (Nicotiana tabacum L.) leaves. J Plant Physiol 166:1057–1068PubMedGoogle Scholar
  67. Ohsumi Y (2001) Molecular dissection of autophagy: two ubiquitin-like systems. Nat Rev Mol Cell Biol 3:211–216Google Scholar
  68. Ono K, Hashimoto H, Katoh S (1995) Changes in the number and size of chloroplasts during senescence of primary leaves of wheat grown under conditions. Plant Cell Physiol 36:9–17Google Scholar
  69. Otegui MS, Noh Y-S, Martinez DE, Petroff MGV, Staehelin LA, Amasino RM, Guiamet JJ (2005) Senescence-associated vacuoles with intense proteolytic activity develop in leaves of Arabidopsis and soybean. Plant J 41:831–844PubMedGoogle Scholar
  70. Park H, Eggink LL, Roberson RW, Hoober JK (1999) Transfer of proteins from the chloroplast to the vacuoles in Chlamydomonas reinhardtii (chlorophyta): a pathway for degradation. J Phycol 35:528–538Google Scholar
  71. Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975:384–394Google Scholar
  72. Prakash JSS, Baig MA, Mohanty P (2001) Senescence induced structural reorganization of thylakoid membranes in Cucumis sativus cotyledons. LHC II involvement in reorganization of thylakoid membranes. Photosynth Res 68:153–161PubMedGoogle Scholar
  73. Prins A, van Heerden P, Olmos E, Kunert K, Foyer C (2008) Cysteine proteinases regulate chloroplast protein content and composition in tobacco leaves: a model for dynamic interactions with ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) vesicular bodies. J Exp Bot 59:1935–1950PubMedGoogle Scholar
  74. Radhamony R, Theg S (2006) Evidence for an ER to Golgi to chloroplast protein transport pathway. Trends Cell Biol 16:385–387PubMedGoogle Scholar
  75. Rascio N, Mariani P, Chitano P, Dalla Vecchia F (1986) An ultrastructural study of maize leaf etioplasts throughout their entire life-cycle. Protoplasma 130:98–107Google Scholar
  76. Saito C, Ueda T, Abe H, Wada Y, Kuroiwa T, Hisada A, Furuya M, Nakano A (2002) A complex and mobile structure forms a distinct subregion within the continuous vacuolar membrane in young cotyledons of Arabidopsis. Plant J 29:245–255PubMedGoogle Scholar
  77. Schmid M, Simpson D, Gietl C (1999) Programmed cell death in castor bean endosperm is associated with the accumulation and release of a cysteine endopeptidase from ricinosomes. Proc Natl Acad Sci USA 96:14159–14164PubMedGoogle Scholar
  78. Simeonova E, Sikora A, Charzynska M, Mostowska A (2000) Aspects of programmed cell death during leaf senescence of mono- and dicotyledonous plants. Protoplasma 214:93–101Google Scholar
  79. Sitte P (1977) Chromoplasten – bunte Objekte der modernen Zellbiologie. BIUZ 7:65–74Google Scholar
  80. Spundova M, Popelkova H, Ilik P, Skotnica J, Novotny R, Naus J (2003) Ultrastructural and functional changes in the chloroplasts of detached barley leaves senescing under dark and light conditions. J Plant Physiol 160:1051–1058PubMedGoogle Scholar
  81. Terai M, Watada A, Murphy C, Wergin W (2000) Scanning electron microscopic study of modified chloroplasts in senescing broccoli florets. Hortscience 35:99–103Google Scholar
  82. Tevini M, Steinmüller D (1985) Composition and function of plastoglobuli. II. Lipid composition of leaves and plastoglobuli during beech leaf senescence. Planta 163:91–96Google Scholar
  83. 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 137:53–60Google Scholar
  84. Thomson WW, Platt-Aloia KA (1987) Ultrastructural changes associated with senescence. In: Thomson WW, Nothnagel EA, Huffaker RC (eds) Plant senescence: its biochemistry and physiology. American Society of Plant Physiologists, Monona DriveGoogle Scholar
  85. Toyooka K, Okamoto T, Minamikawa T (2001) Cotyledon cells of Vigna mungo seedlings use at least two distinct autophagic machineries for degradation of starch granules and cellular components. J Cell Biol 154:973–982PubMedGoogle Scholar
  86. Tuquet C, Newman DW (1980) Aging and regreening in soybean cotyledons. 1. Ultrastructural changes in plastids and plastoglobuli. Cytobios 29:43–59PubMedGoogle Scholar
  87. Uzunova AN, Popova LP (2000) Effect of salicylic acid on leaf anatomy and chloroplast ultrastructure of barley plants. Photosynthetica 38:243–250Google Scholar
  88. Vidi P-A, Kanwischer M, Baginsky S, Austin J, Csucs G, Dörmann P, Kessler F, Bréhélin C (2006) Tocopherol cyclase (VTE1) localization and Vitamin E accumulation in chloroplast plasto­globule lipoprotein particles. J Biol Chem 281:11225–11234PubMedGoogle Scholar
  89. Villarejo A, Buren S, Larsson S, Dejardin A, Monne M, Rudhe C, Karlsson J, Jansson S, Lerouge P, Rolland N, von Heijne G, Grebe M, Bako L, Samuelsson G (2005) Evidence for a protein transported through the secretory pathway en route to the higher plant chloroplast. Nat Cell Biol 12:1224–1231Google Scholar
  90. Wada S, Ishida H, Izumi M, Yoshimoto K, Ohsumi Y, Mae T, Makino A (2009) Autophagy plays a role in chloroplast degradation during senescence in individually darkened leaves. Plant Physiol 149:885–893PubMedGoogle Scholar
  91. Whatley JM, McLean B, Juniper BE (1991) Continuity of chloroplast and endoplasmic-reticulum membranes in Phaseolus vulgaris. New Phytol 117:209–217Google Scholar
  92. Wise RR (2006) The diversity of plastid form and function. The structure and function of plastids. Adv Photosynth Resp 23:3–26Google Scholar
  93. Wittenbach VA, Ackersen RC, Giaquinta RT, Hebert RR (1980) Changes in photosynthesis, ribulose bisphosphate carboxylase, proteolytic activity, and ultrastructure of soybean leaves during senescence. Crop Sci 20:225–231Google Scholar
  94. Wittenbach VA, Lin W, Herbert RR (1982) Vacuolar localization of proteases and degradation of chloroplasts in mesophyll protoplasts from senescing primary wheat leaves. Plant Physiol 69:98–102PubMedGoogle Scholar
  95. Wolf FT (1956) Changes in chlorophyll-a and chlorophyll-b in autumn leaves. Am J Bot 43:714–718Google Scholar
  96. Wredle U, Walles B, Hakman I (2001) DNA fragmentation and nuclear degradation during programmed cell death in the suspensor and endosperm of Vicia faba. Int J Plant Sci 162:1053–1063Google Scholar
  97. Wrischer M, Preberg T, Magnus V, Ljubesic N (2009) Unusual thylakoid structures appearing during degradation of the photosynthetic apparatus in chloroplasts. Acta Bot Croat 68:1–9Google Scholar
  98. Xu Q, Paulsen G, Guikema J, Paulsen G (1995) Func­tional and ultrastructural injury to photosynthesis in wheat by high temperature during maturation. Environ Exp Bot 35:43–54Google Scholar
  99. Yoshimoto K, Jikumaru Y, Kamiya Y, Kusano M, Consonni C, Panstruga R, Ohsumi Y, Shirasu K (2009) Autophagy negatively regulates cell death by controlling NPR1-dependent salicylic acid signaling during senescence and the innate immune response in Arabidopsis. Plant Cell 21:2914–2927PubMedGoogle Scholar
  100. Zavaleta-Mancera HA, Thomas BJ, Thomas H, Scott IM (1999) Regreening of senescent Nicotiana leaves: II. Redifferentiation of plastids. J Exp Bot 50:1683–1689Google Scholar
  101. Zhang MP, Zhang CJ, Yu GH, Jiang YZ, Strasser RJ, Yuan ZY, Yang XS, Chen GX (2010) Changes in chloroplast ultrastructure, fatty acid components of thylakoid membrane and chlorophyll a fluorescence transient in flag leaves of a super-high-yield hybrid rice and its parents during the reproductive stage. J Plant Physiol 167:277–285PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.Institute of Botany, Central MicroscopyUniversity of KielKielGermany

Personalised recommendations