The Dynamic Role of Chloroplasts in Integrating Plant Growth and Development

  • Karin Krupinska
  • Udaya C. Biswal
  • Basanti BiswalEmail author
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 36)


This chapter refers to the entire book and uses the information presented in the individual chapters to provide a brief survey of the current knowledge of plastid development and chloro­plast biology, which reaches far beyond the photosynthetic function of the organelle. The organelle significantly modulates plant growth, development and senescence. The development of chloro­plasts is closely associated with the development of the whole plant. Its development involves both nuclear and plastid gene expression and environmental modulation. Although the levels of transcriptional and post-transcriptional control of gene expression and the import of nuclear encoded proteins into the organelle have been studied intensively, the coordinated assembly of the multimeric complexes, required for chloroplast function, still remains a mystery. New ideas are emerging on the expression potential of plastid DNA, its stability and regulation during development of the organelle. The regulation of chloroplast development involves interactions of cellular organelles, exchange of metabolites, participation of phytohormones, reactive oxygen species (ROS) and intensive cross-talk with the nucleus (anterograde and retrograde signaling). Chloroplast development begins with proplastid-to-chloroplast transformation that involves coordinated synthesis of lipids, proteins and pigments. In multimeric protein complexes bound to thylakoids or located in the stroma, the proteins and cofactors assemble in sequence with a definite stoichiometry. On the other hand, transformation of mature chloroplasts to gerontoplasts during leaf senescence causes regulated disassembly of the structural fabric of the organelle with loss in photosynthesis. The mechanisms of senescence induced degradation of pigments, proteins and lipids follow distinct pathways. The enzymes involved in the degrada­tion are largely known. The degradation pathways occur inside and outside of plastids; the latter is mediated by autophagy, participation of senescence associated vacuoles (SAVs) and Rubisco containing bodies (RCBs). The process is associated with expression of senescence associated genes (SAGs). Chloroplasts, both during biogenesis and senescence, respond to the environmental changes and adapt with appropriate modifications, in response to the changes. Finally, in this chapter we have raised several unanswered questions to be addressed in the future and have provided a critical discussion on the direction of further research in the area.


Thylakoid Membrane Chloroplast Development Plastid Gene Plastid Protein Chloroplast Biogenesis 
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.



Abscisic acid;


Endoplasmic reticulum;


Green fluorescent protein;


Jasmonic acid;


Nuclear encoded phage-type RNA polymerase;


Plastid encoded RNA polymerase;


Photosystem I;


Photosystem II;


Rubisco containing bodies;


Reactive oxygen species;


Ribulose bis phosphate carboxylase oxygenase;


Salicylic acid; SAGs – Senescence associated genes;


Senescence associated vacuoles;


Translocon of the inner envelope membrane of chloroplast;


Translocon of the outer envelope membrane of chloroplast;


Trehalose 6-phosphate



Research of Karin Krupinska on plastid biology and leaf senescence is supported by the German Research Foundation (DFG) and the European Community (EC). Basanti Biswal wishes to thank Defence Research and Development Organization (DRDO) and Council of Scientific and Industrial Research (CSIR), New Delhi for financial support.


  1. Abreu I, Santos A (1977) Intimate association between endoplasmic reticulum and plastids during microsporogenesis in Lycopersicum esculentum Mill. and Solanum tuberosum L. J Submicrosc Cytol Pathol 9:239–246Google Scholar
  2. Amunts A, Toporik H, Borovikova A, Nelson N (2010) Structure determination and improved model of plant photosystem I. J Biol Chem 285:3478–3486PubMedCrossRefGoogle Scholar
  3. Anderson JM, Chow WS, Park YI (1995) The grand design of photosynthesis: acclimation of photosynthetic apparatus to environmental cues. Photosynth Res 46:129–139CrossRefGoogle Scholar
  4. Andersson MX, Goksör M, Sandelius AS (2007) Optical manipulation reveals strong attracting forces at membrane contact sites between endoplasmic reticulum and chloroplasts. J Biol Chem 282:1170–1174PubMedCrossRefGoogle Scholar
  5. Bayer RG, Stael S, Csaszar E, Teige M (2011) Mining the soluble chloroplast proteome by affinity chromatography. Proteomics 11:1287–1299PubMedCrossRefGoogle Scholar
  6. Biswal B, Joshi PN, Raval MK, Biswal UC (2011) Photosynthesis, a global sensor of environmental stress in green plants: stress signaling and adaptation. Curr Sci 101:47–56Google Scholar
  7. Biswal UC, Biswal B (1988) Ultrastructural modifications and biochemical changes during senescence of chloroplasts. Int Rev Cytol 113:271–321CrossRefGoogle Scholar
  8. Biswal UC, Biswal B, Raval MK (2003) Chloroplast biogenesis: from proplastid to gerontoplast. Springer, DordrechtCrossRefGoogle Scholar
  9. Boffey SA, Selldén G, Leech RM (1980) Influence of cell age on chlorophyll formation in light-grown and etiolated wheat seedlings. Plant Physiol 65:680–684PubMedCrossRefGoogle Scholar
  10. Bracher A, Starling-Windhof A, Hartl FU, Hayer-Hartl M (2011) Crystal structure of a chaperone-bound assembly intermediate of form I Rubisco. Nat Struct Mol Biol 18:875–880PubMedCrossRefGoogle Scholar
  11. Carrie C, Giraud E, Whelan J (2009) Protein transport in organelles: dual targeting of proteins to mitochondria and chloroplasts. FEBS J 276:1187–1195PubMedCrossRefGoogle Scholar
  12. 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 44:914–921PubMedCrossRefGoogle Scholar
  13. Crotty WJ, Ledbette MC (1973) Membrane continuities involving chloroplasts and other organelles in plant cells. Science 182:839–841PubMedCrossRefGoogle Scholar
  14. Duchêne AM, Giritch A, Hoffmann B, Cognat V, Lancelin D, Peeters NM, Zaepfel M, Marechal-Drouard L, Small ID (2005) Dual targeting is the rule for organellar aminoacyl-tRNA synthetases in Arabidopsis thaliana. Proc Natl Acad Sci USA 102:16484–16489PubMedCrossRefGoogle Scholar
  15. Eckardt NA (2007) Thylakoid development from biogenesis to senescence, and ruminations on regulation. Plant Cell 19:1135–1138CrossRefGoogle Scholar
  16. Ensminger I, Busch F, Huner NPA (2006) Photostasis and cold acclimation: sensing low temperature through photosynthesis. Physiol Plant 126:28–44CrossRefGoogle Scholar
  17. Esau K (1944) Anatomical and cytological studies on beet mosaic. J Agric Res 69:95–117Google Scholar
  18. Feller U, Anders I, Mae T (2007) Rubiscolytics: fate of Rubisco after its enzymatic function in a cell is terminated. J Exp Bot 59:1615–1624PubMedCrossRefGoogle Scholar
  19. Gibbs S (1981) The chloroplast endoplasmic reticulum: structure, function, and evolutionary significance. Int Rev Cytol 72:49–99CrossRefGoogle Scholar
  20. Grabowski E, Miao Y, Mulisch M, Krupinska K (2008) Single-stranded DNA binding protein Whirly1 in barley leaves is located in plastids and the nucleus of the same cell. Plant Physiol 147:1800–1804PubMedCrossRefGoogle Scholar
  21. Gray JC, Hansen MR, Shaw DJ, Graham K, Dale R, Smallman P, Natesan SKA, Newell CA (2011) Plastid stromules are induced by stress treatments acting through abscisic acid. Plant J 69:387–398PubMedCrossRefGoogle Scholar
  22. Gunning BES (2005) Plastid stromules: video microscopy of their outgrowth, retraction, tensioning, anchoring, bridging, and tip-shedding. Protoplasma 225:33–42PubMedCrossRefGoogle Scholar
  23. Hörtensteiner S (2007) Chlorophyll degradation during senescence. Annu Rev Plant Biol 57:55–77CrossRefGoogle Scholar
  24. Hörtensteiner S, Kräutler B (2011) Chlorophyll breakdown in higher plants. Biochim Biophys Acta 1807:977–988PubMedCrossRefGoogle Scholar
  25. Inaba T, Ito-Inaba Y (2010) Versatile roles of plastids in plant growth and development. Plant Cell Physiol 51:1847–1853PubMedCrossRefGoogle Scholar
  26. Isemer R, Mulisch M, Schäfer A, Kirchner S, Koop HU, Krupinska K (2012) Recombinant Whirly1 translocates from transplastomic chloroplasts to the nucleus. FEBS Lett 586:85–88PubMedCrossRefGoogle Scholar
  27. Jarvis P (2008) Targeting of nucleus-encoded proteins to chloroplasts in plants. New Phytol 179:257–285PubMedCrossRefGoogle Scholar
  28. Kato Y, Sakamoto W (2010) New insights into the types and function of proteases in plastids. In: Kwang WJ (ed) International review of cell and molecular biology, vol 161. Burlington Academic Press, Burlington, pp 185–218Google Scholar
  29. Köhler RH, Cao J, Zipfel WR, Webb WW, Hanson MO (1997) Exchange of protein molecules through connections between higher plant plastids. Science 276:2039–2042PubMedCrossRefGoogle Scholar
  30. Krause K, Krupinska K (2009) Nuclear regulators with a second home in organelles. Trends Plant Sci 14:194–199PubMedCrossRefGoogle Scholar
  31. Krenz B, Windeisen V, Wege C, Jeske H, Kleinow T (2010) A plastid-targeted heat shock cognate 70kDa protein interacts with the Abutilon mosaic virus movement protein. Virology 401:6–17PubMedCrossRefGoogle Scholar
  32. Krupinska K, Humbeck K (2004) Photosynthesis and chloroplast breakdown (Review). In: Noóden LD (ed) Plant cell death processes. Elsevier Academic Press, San Diego, pp 169–188CrossRefGoogle Scholar
  33. Kwak MJ, Lee SH, Woo SY (2011) Growth and anatomical characteristics of different water and light intensities on cork oak (Quercus suber L.) seedlings. Afr J Biotechnol 10:10964–10979CrossRefGoogle Scholar
  34. Li HM, Chiu CC (2010) Protein transport into chloroplasts. Annu Rev Plant Biol 61:157–180PubMedCrossRefGoogle Scholar
  35. Lichtenthaler HK (1969) Die Plastoglobuli von Spinat, ihre Größe und Zusammensetzung während der Chloroplastendegeneration. Protoplasma 68:315–326CrossRefGoogle Scholar
  36. Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annu Rev Plant Biol 58:115–136PubMedCrossRefGoogle Scholar
  37. Ling Q, Huang W, Baldwin A, Jarvis P (2012) Chloroplast biogenesis is regulated by direct action of the ubiquitin-proteasome system. Science 338:655–659PubMedCrossRefGoogle Scholar
  38. Liu C, Young AL, Starling-Windhof A, Bracher A, Saschenbrecker S, Rao BV, Rao KV, Berninghausen O, Mielke T, Hartl FU, Beckmann R, Hayer-Hartl M (2010) Coupled chaperone action in folding and assembly of hexadecameric Rubisco. Nature 463:197–202PubMedCrossRefGoogle Scholar
  39. López-Juez E (2007) Plastid biogenesis, between light and shadows. J Exp Bot 58:11–26PubMedCrossRefGoogle Scholar
  40. López-Juez E, Pyke KA (2005) Plastids unleashed: their development and their integration in plant development. Int J Dev Biol 49:557–577PubMedCrossRefGoogle Scholar
  41. Mathur J, Radhamony R, Sinclair AM, Donoso A, Dunn N, Roach E, Radford D, Mohaghegh SM, Logan DC, Kokolic K, Mathur N (2010) mEosFP-Based green-to-red photoconvertible subcellular probes for plants. Plant Physiol 154:1573–1587PubMedCrossRefGoogle Scholar
  42. Mur LA, Aubry S, Mondhe M, Kingston-Smith A, Gallagher J, Timms-Taravella E, James C, Papp I, Hörtensteiner S, Thomas H, Ougham H (2010) Accumulation of chlorophyll catabolites photosensitizes the hypersensitive response elicited by Pseudomonas syringae in Arabidopsis. New Phytol 188:161–174PubMedCrossRefGoogle Scholar
  43. Nixon PJ, Michoux F, Yu J, Boehm M, Komenda J (2010) Recent advances in understanding the assembly and repair of photosystem II. Ann Bot 106:1–16PubMedCrossRefGoogle Scholar
  44. 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 41:831–844PubMedCrossRefGoogle Scholar
  45. Ougham H, Hörtensteiner S, Armstead I, Donnison I, King I, Thomas H, Mur L (2008) The control of chlorophyll catabolism and the status of yellowing as a biomarker of leaf senescence. Plant Biol 10:4–14PubMedCrossRefGoogle Scholar
  46. Ozawa S, Nield J, Terao A, Stauber EJ, Hippler M, Koike H, Rochaix J, Takahashi Y (2009) Biochemical and structural studies of the large Ycf4-photosystem I assembly complex of the green alga Chlamydomonas reinhardtii. Plant Cell 21:2424–2442PubMedCrossRefGoogle Scholar
  47. Padmasree K, Padmavathi L, Raghavendra A (2002) Essentiality of mitochondrial oxidative metabolism for photosynthesis: optimization of carbon assimilation and protection against photoinhibition. Crit Rev Biochem Mol Biol 37:71–119PubMedCrossRefGoogle Scholar
  48. Pogson BJ, Albrecht V (2011) Genetic dissection of chloroplast biogenesis and development: an overview. Plant Physiol 155:1545–1551PubMedCrossRefGoogle Scholar
  49. Raab S, Toth Z, de Groot C, Stamminger T, Hoth S (2006) ABA-responsive RNA binding proteins are involved in chloroplast and stromule function in Arabidopsis seedlings. Planta 224:900–914PubMedCrossRefGoogle Scholar
  50. Richter S, Lamppa GK (1998) A chloroplast processing enzyme functions as a general stromal peptidase. Proc Natl Acad Sci USA 95:7463–7468PubMedCrossRefGoogle Scholar
  51. Rochaix JD (2011) Assembly of the photosynthetic apparatus. Plant Physiol 155:1493–1500PubMedCrossRefGoogle Scholar
  52. Sakai A, Takano H, Kuroiwa T (2004) Organelle nuclei in higher plants: structure, composition, function and evolution. Int Rev Cytol 238:59–118PubMedCrossRefGoogle Scholar
  53. Saschenbrecker S, Bracher A, Rao KV, Rao BV, Hartl FU, Hayer-Hartl M (2007) Structure and function of RbcX, an assembly chaperone for hexadecameric Rubisco. Cell 129:1189–1200PubMedCrossRefGoogle Scholar
  54. Schöttler MA, Albus CA, Bock R (2011) Photosystem I: its biogenesis and function in higher plants. J Plant Physiol 168:1452–1461PubMedCrossRefGoogle Scholar
  55. Sitte P (1977) Chromoplasten – bunte Objekte-der modernen Zellbiologie. BIUZ 7:65–74CrossRefGoogle Scholar
  56. Small I, Wintz H, Akashi K, Mireau H (1998) Two birds with one stone: genes that encode products targeted to two or more compartments. Plant Mol Biol 38:265–277PubMedCrossRefGoogle Scholar
  57. Soll J, Schleiff E (2004) Protein import into chloroplasts. Nat Rev Mol Cell Biol 5:198–208PubMedCrossRefGoogle Scholar
  58. Thomas H, Ougham HJ, Wagstaff C, Stead AD (2003) Defining senescence and death. J Exp Bot 54:1127–1132PubMedCrossRefGoogle Scholar
  59. Umena Y, Kawakami K, Shen JR, Kamiya K (2011) Crystal structure of oxygen evolving photosystem II at a resolution of 1.9 Å. Nature 473:55–60PubMedCrossRefGoogle Scholar
  60. Van Doorn WG, Woltering EJ (2004) Senescence and programmed cell death: substance or semantics? J Exp Bot 55:2147–2153PubMedCrossRefGoogle Scholar
  61. Van Doorn WG, Yoshimoto K (2010) Role of chloroplasts and other plastids in ageing and death of plants and animals: a tale of Vishnu and Shiva. Ageing Res Rev 9:117–130PubMedCrossRefGoogle Scholar
  62. Villarejo A, Burén S, Larsson S, Déjardin A, Monné 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 12:1224–1231CrossRefGoogle Scholar
  63. Wellburn AR, Hampp R (1976) Movement of labelled metabolites from mitochondria to plastids during development. Planta 131:17–20CrossRefGoogle Scholar
  64. Whatley JM, McLean B, Juniper BE (1991) Continuity of chloroplast and endoplasmic reticulum membranes in Phaseolus Vulgaris. New Phytol 117:209–217CrossRefGoogle Scholar
  65. Wildman SG, Hongladarom T, Honda SI (1962) Chloroplasts and mitochondria in living plant cells: cinephotomicrographic studies. Science 138:434–436PubMedCrossRefGoogle Scholar
  66. Wingler A, Purdy S, MacLean JA, Pourtau N (2006) The role of sugars in integrating environmental signals during the regulation of leaf senescence. J Exp Bot 57:391–399PubMedCrossRefGoogle Scholar
  67. Wingler A, Delatte TL, O’Hara LE, Primavesi LF, Jhurreea D, Paul MJ, Schluepmann H (2012) Trehalose 6-phosphate is required for the onset of leaf senescence associated with high carbon availability. Plant Physiol 158:1241–1251PubMedCrossRefGoogle Scholar
  68. Wise RR, Hoober JK (eds) (2006) The structure and function of plastids. Springer, The NetherlandsGoogle Scholar
  69. Wooding FB, Northcote DH (1965) The fine structure of the mature resin canal cells of Pinus pinea. J Ultrastruct Res 13:233–244PubMedCrossRefGoogle Scholar
  70. Xu C, Fan J, Riekhof W, Froehlich JE, Benning C (2003) A permease-like protein involved in ER to thylakoid lipid transfer in Arabidopsis. EMBO J 22:2370–2379PubMedCrossRefGoogle Scholar
  71. Zhelyazkova P, Sharma CM, Förstner KU, Liere K, Vogel J, Börner T (2012) The primary transcriptome of barley chloroplasts: numerous noncoding RNAs and the dominating role of the plastid-encoded RNA polymerase. Plant Cell 24:123–136PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Karin Krupinska
    • 1
  • Udaya C. Biswal
    • 2
  • Basanti Biswal
    • 2
    Email author
  1. 1.Institute of BotanyUniversity of KielKielGermany
  2. 2.School of Life SciencesSambalpur UniversitySambalpurIndia

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