Skip to main content

Ultrastructural Analyses of Senescence Associated Dismantling of Chloroplasts Revisited

  • Chapter
  • First Online:
Plastid Development in Leaves during Growth and Senescence

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 36))

Summary

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.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 259.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 329.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 329.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

ATG genes –:

Autophagy related genes;

CLSM:

Confocal laser scanning microscopy;

cv.:

Cultivar;

EM:

Electron microscopy;

ER:

Endoplasmic reticulum;

GFP:

Green fluorescence protein;

h D:

Hours in darkness;

h L:

Hours in light;

PPV:

Precursor protease vesicle(s);

PSV:

Protein storage vesicle(s);

RCB:

Rubisco-containing body(s);

RCV:

Rubisco-containing vesicle(s);

rER:

Rough endoplasmic reticulum;

Rubisco:

Ribulose-1,5-bisphosphate carboxylase oxygenase;

SAV:

Senescence-associated vacuole;

TIP:

Tonoplast intrinsic protein

References

  • Anderson JM (1999) Insights into the consequence of grana stacking of thylakoid membranes in vascular plants: a personal perspective. Aust J Plant Physiol 26:625–639

    CAS  Google Scholar 

  • Anderson JM, Andersson B (1982) The architecture of photosynthetic membranes – lateral and transverse organization. Trends Biochem Sci 7:288–292

    CAS  Google Scholar 

  • 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 282:1170–1174

    PubMed  CAS  Google Scholar 

  • Andrade-Navarro MA, Sanchez-Pulido L, McBride HM (2009) Mitochondrial vesicles: an ancient process providing new links to peroxisomes. Curr Opin Cell Biol 21:560–567

    PubMed  CAS  Google Scholar 

  • 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 18:1693–1703

    PubMed  CAS  Google Scholar 

  • Barton R (1966) Fine structure of mesophyll cells in senescing leaves of Phaseolus. Planta 71:314–325

    Google Scholar 

  • Bayer RG, Stael S, Csaszar E, Teige M (2011) Mining the soluble chloroplast proteome by affinity chromatography. Proteomics 11:1287–1299

    PubMed  CAS  Google Scholar 

  • Benning C, Xu CC, Awai K (2006) Non-vesicular and vesicular lipid trafficking involving plastids. Curr Opin Plant Biol 9:241–247

    PubMed  CAS  Google Scholar 

  • Biswal UC, Biswal B (1988) Ultrastructural modifications and biochemical changes during senescence of chloroplasts. Int Rev Cytol 113:271–321

    CAS  Google Scholar 

  • Biswal UC, Biswal B, Raval MK (2003) Chloroplast biogenesis: from proplastid to gerontoplast. Kluwer, Dordrecht

    Google Scholar 

  • Butler RD (1967) The fine structure of senescing cotyledons of cucumber. J Exp Bot 18:535–543

    Google Scholar 

  • Camp PJ, Huber SC, Burke JJ, Moreland DE (1982) Biochemical changes that occur during senescence of wheat leaves. Plant Physiol 70:1641–1646

    PubMed  CAS  Google Scholar 

  • 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 44:914–921

    PubMed  CAS  Google Scholar 

  • Chonan N, Kawahara H, Matsuda T (1977) Changes in chloroplast ultrastructure during senescence of leaves in rice plants. Jap J Crop Sci 46:379–386

    Google Scholar 

  • 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 171–176

    Google Scholar 

  • Crotty WJ, Ledbetter MC (1973) Membrane continuities involving chloroplasts and other organelles in plant cells. Science 182:839–841

    PubMed  CAS  Google Scholar 

  • 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 119:19–29

    CAS  Google Scholar 

  • Eilam Y, Butler RD, Simon EW (1971) Ribosomes and polysomes in cucumber leaves during growth and senescence. Plant Physiol 47:317–323

    PubMed  CAS  Google Scholar 

  • 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 540:35–40

    PubMed  CAS  Google Scholar 

  • Gärtner P-J, Nagl W (1980) Acid phosphatase activity in plastids (plastolysomes) of senescing embryo-suspensor cells. Planta 149:341–349

    Google Scholar 

  • Gepstein S (1988) Photosynthesis. In: Noodén LD, Leopold AC (eds) Senescence and aging in plants. Academic, San Diego, pp 85–111

    Google Scholar 

  • Ghosh S, Hudak K, Dumbroff EB, Thompson JE (1994) Release of photosynthetic catabolites by blebbing from thylakoids. Plant Physiol 106:1547–1553

    PubMed  CAS  Google Scholar 

  • Ghosh S, Mahoney SR, Penterman JN, Peirson D, Dumbroff EB (2001) Ultrastructural and biochemical changes in chloroplasts during Brassica napus senescence. Plant Physiol Biochem 39:777–784

    Google Scholar 

  • Gibbs S (1981) The chloroplast endoplasmic reticulum: structure, function, and evolutionary significance. Int Rev Cytol 72:49–99

    Google Scholar 

  • 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 102:2238–2243

    CAS  Google Scholar 

  • Guiamet JJ, Pichersky E, Nooden LD (1999) Mass exodus from senescing soybean chloroplasts. Plant Cell Physiol 40:986–992

    CAS  Google Scholar 

  • Gunning BES (2005) Plastid stromules: video microscopy of their outgrowth, retraction, tensioning, anchoring, bridging, and tip-shedding. Protoplasma 225:33–42

    PubMed  Google Scholar 

  • Harris JB (1978) Development of a tubular apparatus in chloroplasts of aging Cyphomandra leaves. Cytobios 21:151–164

    PubMed  CAS  Google Scholar 

  • Harris JB, Arnott HJ (1973) Effects of senescence on chloroplasts of tobacco leaf. Tissue Cell 5:527–544

    PubMed  CAS  Google Scholar 

  • Harris JB, Schaefer VG (1981) Some correlated events in aging leaf tissue of tree tomato and tobacco. Botanica Gazetta 142:43–54

    CAS  Google Scholar 

  • 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 30:707–777

    CAS  Google Scholar 

  • 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 56:1117–1128

    PubMed  CAS  Google Scholar 

  • Hernandez VJ, Schaedle M (1973) Functional and structural changes in senescing Populus deltoides (Batr.) chloroplasts. Plant Physiol 51:245–249

    Google Scholar 

  • Huber DJ, Newman DW (1976) Relationship between lipid changes and plastid ultrastructural changes in senescing and regreening soybean cotyledons. J Exp Bot 27:490–511

    CAS  Google Scholar 

  • 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 19:337–344

    CAS  Google Scholar 

  • Hurkman WJ (1979) Ultrastructural changes of chloroplasts in attached and detached, aging primary wheat leaves. Am J Bot 66:64–70

    Google Scholar 

  • 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 148:142–155

    PubMed  CAS  Google Scholar 

  • 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 22:217–227

    CAS  Google Scholar 

  • Kolodziejek I, Waleza M, Mostowska A (2006) Morphological, histochemical and ultrastructural indicators of maize and barley leaf senescence. Biol Plant 50:565–573

    Google Scholar 

  • 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 433–449

    Google Scholar 

  • Krupinska K (2011) Plastiden und Zellkern im Zwiegespräch. BIUZ 41:298–305

    CAS  Google Scholar 

  • 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 144:189–200

    PubMed  CAS  Google Scholar 

  • Kunst L, Wrischer M (1984) Adaptational changes of plastids in the leaves of Ligustrum ovalifolium Hassk var aureum at different light intensities. Protoplasma 122:132–137

    Google Scholar 

  • 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 31:33–38

    Google Scholar 

  • Kutik J (1998) The development of chloroplast structure during leaf ontogeny. Photosynthetica 35:481–505

    CAS  Google Scholar 

  • Lichtenthaler HK (1966) Verbreitung und Konzentration des a-Tocopherols in Chloroplasten. Ber Dtsch Bot Ges 79:111–117

    CAS  Google Scholar 

  • Lichtenthaler HK (1968) Plastoglobules and the fine structure of plastids. Endeavour 27:144–149

    CAS  Google Scholar 

  • Lichtenthaler HK (1969) Die Plastoglobuli von Spinat, ihre Größe und Zusammensetzung während der Chloroplastendegeneration. Protoplasma 68:315–326

    CAS  Google Scholar 

  • Lichtenthaler HK (1970) Die Lokalisation der Plastidenchinone in den Chromoplasten der Petalen von Sarothamnus scoparius (L) Wimm ex Koch. Planta 90:142–152

    CAS  Google Scholar 

  • Lichtenthaler HK, Sprey B (1966) Ultrastructural changes in chloroplasts of detached parsley leaves. Z Naturforsch 21b:690–697

    Google Scholar 

  • Lichtenthaler HK, Weinert H (1970) Die Beziehungen ­zwischen Lipochinonbiosynthese und Plastoglo­bulibildung in den Chloroplasten von Ficus elastica Roxb. Zeitschrift für Naturforschung 25b:619–623

    Google Scholar 

  • LjubeÅ¡ić N (1968) Feinbau der Chloroplasten während der Vergilbung und Wiederergrünung der Blätter. Protoplasma 66:369–379

    Google Scholar 

  • 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 25:333–336

    CAS  Google Scholar 

  • Martínez DE, Costa ML, Guiamet JJ (2008) Senescence-associated degradation of chloroplast proteins inside and outside the organelle. Plant Biol 10:15–22

    PubMed  Google Scholar 

  • Matile P (1975) The lytic compartment of plant cells. Cell Biology Monographs, vol. 1, Springer, Berlin

    Google Scholar 

  • Matile P (1992) Chloroplast senescence. In: Baker NR, Thomas H (eds) Crop photosynthesis: spatial and temporal determinants. Elsevier, Amsterdam, pp 423–440

    Google Scholar 

  • Matile P (1997) The vacuole and cell senescence. Adv Bot Res 25:87–112

    CAS  Google Scholar 

  • 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 218:144–153

    PubMed  CAS  Google Scholar 

  • 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 73:239–252

    Google Scholar 

  • Mlodzianowski F (1975) Ultrastrucutral changes in chloroplasts of Populis tremula L., leaves affected by the fungus Melampsora pinitorqua Braun. Rostr. Physiol Plant Pathol 6:1–3

    Google Scholar 

  • 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:649–656

    Google Scholar 

  • 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 69:13–25

    CAS  Google Scholar 

  • 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 6:1–3

    Google Scholar 

  • 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 23:677–685

    PubMed  CAS  Google Scholar 

  • 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 18:102–108

    PubMed  CAS  Google Scholar 

  • 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 166:1057–1068

    PubMed  CAS  Google Scholar 

  • Ohsumi Y (2001) Molecular dissection of autophagy: two ubiquitin-like systems. Nat Rev Mol Cell Biol 3:211–216

    Google Scholar 

  • 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 36:9–17

    CAS  Google Scholar 

  • 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 41:831–844

    PubMed  CAS  Google Scholar 

  • 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 35:528–538

    CAS  Google Scholar 

  • 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 975:384–394

    CAS  Google Scholar 

  • 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 68:153–161

    PubMed  CAS  Google Scholar 

  • 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 59:1935–1950

    PubMed  CAS  Google Scholar 

  • Radhamony R, Theg S (2006) Evidence for an ER to Golgi to chloroplast protein transport pathway. Trends Cell Biol 16:385–387

    PubMed  CAS  Google Scholar 

  • Rascio N, Mariani P, Chitano P, Dalla Vecchia F (1986) An ultrastructural study of maize leaf etioplasts throughout their entire life-cycle. Protoplasma 130:98–107

    Google Scholar 

  • 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 29:245–255

    PubMed  Google Scholar 

  • 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 96:14159–14164

    PubMed  CAS  Google Scholar 

  • Simeonova E, Sikora A, Charzynska M, Mostowska A (2000) Aspects of programmed cell death during leaf senescence of mono- and dicotyledonous plants. Protoplasma 214:93–101

    Google Scholar 

  • Sitte P (1977) Chromoplasten – bunte Objekte der modernen Zellbiologie. BIUZ 7:65–74

    Google Scholar 

  • 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 160:1051–1058

    PubMed  CAS  Google Scholar 

  • Terai M, Watada A, Murphy C, Wergin W (2000) Scanning electron microscopic study of modified chloroplasts in senescing broccoli florets. Hortscience 35:99–103

    Google Scholar 

  • Tevini M, Steinmüller D (1985) Composition and function of plastoglobuli. II. Lipid composition of leaves and plastoglobuli during beech leaf senescence. Planta 163:91–96

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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 Drive

    Google Scholar 

  • 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 154:973–982

    PubMed  CAS  Google Scholar 

  • Tuquet C, Newman DW (1980) Aging and regreening in soybean cotyledons. 1. Ultrastructural changes in plastids and plastoglobuli. Cytobios 29:43–59

    PubMed  CAS  Google Scholar 

  • Uzunova AN, Popova LP (2000) Effect of salicylic acid on leaf anatomy and chloroplast ultrastructure of barley plants. Photosynthetica 38:243–250

    CAS  Google Scholar 

  • 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 281:11225–11234

    PubMed  CAS  Google Scholar 

  • 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 12:1224–1231

    Google Scholar 

  • 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 149:885–893

    PubMed  CAS  Google Scholar 

  • Whatley JM, McLean B, Juniper BE (1991) Continuity of chloroplast and endoplasmic-reticulum membranes in Phaseolus vulgaris. New Phytol 117:209–217

    Google Scholar 

  • Wise RR (2006) The diversity of plastid form and function. The structure and function of plastids. Adv Photosynth Resp 23:3–26

    Google Scholar 

  • 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 20:225–231

    CAS  Google Scholar 

  • 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 69:98–102

    PubMed  CAS  Google Scholar 

  • Wolf FT (1956) Changes in chlorophyll-a and chlorophyll-b in autumn leaves. Am J Bot 43:714–718

    CAS  Google Scholar 

  • 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 162:1053–1063

    Google Scholar 

  • Wrischer M, Preberg T, Magnus V, Ljubesic N (2009) Unusual thylakoid structures appearing during degradation of the photosynthetic apparatus in chloroplasts. Acta Bot Croat 68:1–9

    CAS  Google Scholar 

  • 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 35:43–54

    Google Scholar 

  • 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 21:2914–2927

    PubMed  CAS  Google Scholar 

  • Zavaleta-Mancera HA, Thomas BJ, Thomas H, Scott IM (1999) Regreening of senescent Nicotiana leaves: II. Redifferentiation of plastids. J Exp Bot 50:1683–1689

    CAS  Google Scholar 

  • 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 167:277–285

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Karin Krupinska .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Mulisch, M., Krupinska, K. (2013). Ultrastructural Analyses of Senescence Associated Dismantling of Chloroplasts Revisited. In: Biswal, B., Krupinska, K., Biswal, U. (eds) Plastid Development in Leaves during Growth and Senescence. Advances in Photosynthesis and Respiration, vol 36. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-5724-0_14

Download citation

Publish with us

Policies and ethics