Abstract
Chloroplasts are double membrane bound organelles that are found in plants and algae. Their division requires a number of proteins to assemble into rings along the center of the organelle and to constrict in synchrony. Chloroplasts possess a third membrane system, the thylakoids, which house the majority of proteins responsible for the light-dependent reactions. The mechanism that allows chloroplasts to sort out and separate the intricate thylakoid membrane structures during organelle division remain unknown. By characterizing the sizes of thylakoids found in a number of different chloroplast division mutants in Arabidopsis, we show that thylakoids do not divide independently of the chloroplast division cycle. More specifically, we show that thylakoid division requires the formation of both the inner and the outer contractile rings of the chloroplast.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All data are contained within the article.
References
Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in beta vulgaris. Plant Physiol 24(1):1–15
Austin JR 2nd, Staehelin LA (2011) Three-dimensional architecture of grana and stroma thylakoids of higher plants as determined by electron tomography. Plant Physiol 155(4):1601–1611. https://doi.org/10.1104/pp.110.170647
Bailleul B, Cardol P, Breyton C (2010) Electrochromism: a useful probe to study algal photosynthesis. Photosynth Res 110(2):179–189. https://doi.org/10.1007/s11120-011-9704-7
Boardman NK, Thorne SW, Anderson JM (1966) Fluorescence properties of particles obtained by digitonin fragmentation of spinach chloroplasts. Proc Natl Acad Sci U S A 56(2):586. https://doi.org/10.1073/pnas.56.2.586
Boekema EJ, van Breemen JFL, van Roon H, Dekker JP (2000) Arrangement of photosystem II supercomplexes in crystalline macrodomains within the thylakoid membrane of green plant chloroplasts. J Mol Biol 301(5):1123–1133. https://doi.org/10.1006/jmbi.2000.4037
Burch-Smith TM, Schiff M, Caplan JL, Tsao J, Czymmek K, Dinesh-Kumar SP (2007) A novel role for the TIR domain in association with pathogen-derived elicitors. PLoS Biol 5(3):501–514. https://doi.org/10.1371/journal.pbio.0050068
Chen C, Cao L, Yang Y, Porter KJ, Osteryoung KW (2019) ARC3 activation by PARC6 promotes FtsZ-ring remodeling at the chloroplast division site. Plant Cell 31(4):862–885. https://doi.org/10.1105/tpc.18.00948
Chen C, MacCready JS, Ducat DC, Osteryoung KW (2018) The molecular machinery of chloroplast division. Plant Physiol 176(1):138–151. https://doi.org/10.1104/pp.17.01272
Chen YL, Asano T, Fujiwara MT, Yoshida S, Machida Y, Yoshioka Y (2009) Plant cells without detectable plastids are generated in the crumpled leaf mutant of Arabidopsis thaliana. Plant Cell Physiol 50(5):956–969. https://doi.org/10.1093/Pcp/Pcp047
Chuartzman SG, Nevo R, Shimoni E, Charuvi D, Kiss V, Ohad I, Brumfeld V, Reich Z (2008) Thylakoid membrane remodeling during state transitions in Arabidopsis. Plant Cell 20(4):1029–1039. https://doi.org/10.1105/tpc.107.055830
Daum B, Kuhlbrandt W (2011) Electron tomography of plant thylakoid membranes. J Exp Bot 62(7):2393–2402. https://doi.org/10.1093/Jxb/Err034
Daum B, Nicastro D, Il JA, McIntosh JR, Kuhlbrandt W (2010) Arrangement of photosystem II and ATP synthase in chloroplast membranes of spinach and pea. Plant Cell 22(4):1299–1312. https://doi.org/10.1105/tpc.109.071431
El-Kafafi ES, Karamoko M, Pignot-Paintrand I, Grunwald D, Mandaron P, Lerbs-Mache S, Falconet D (2008) Developmentally regulated association of plastid division protein FtsZ1 with thylakoid membranes in Arabidopsis thaliana. Biochem J 409:87–94. https://doi.org/10.1042/Bj20070543
Fitzpatrick LM, Keegstra K (2001) A method for isolating a high yield of Arabidopsis chloroplasts capable of efficient import of precursor proteins. Plant J 27(1):59–65
Forth D, Pyke KA (2006) The suffulta mutation in tomato reveals a novel method of plastid replication during fruit ripening. J Exp Bot 57(9):1971–1979. https://doi.org/10.1093/jxb/erj144
Fujiwara MT, Yasuzawa M, Kojo KH, Niwa Y, Abe T, Yoshida S, Nakano T, Itoh RD (2018) The Arabidopsis arc5 and arc6 mutations differentially affect plastid morphology in pavement and guard cells in the leaf epidermis. PLoS One 13(2):e0192380. https://doi.org/10.1371/journal.pone.0192380
Gao H, Sage TL, Osteryoung KW (2006) FZL, an FZO-like protein in plants, is a determinant of thylakoid and chloroplast morphology. Proc Natl Acad Sci U S A 103(17):6759–6764. https://doi.org/10.1073/pnas.0507287103
Glynn JM, Froehlich JE, Osteryoung KW (2008) Arabidopsis ARC6 coordinates the division machineries of the inner and outer chloroplast membranes through interaction with PDV2 in the intermembrane space. Plant Cell 20(9):2460–2470. https://doi.org/10.1105/tpc.108.061440
Gu L, Grodzinski B, Han J, Marie T, Zhang YJ, Song YC, Sun Y (2022) Granal thylakoid structure and function: explaining an enduring mystery of higher plants. New Phytol 236(2):319–329. https://doi.org/10.1111/nph.18371
Gupta TK, Klumpe S, Gries K, Heinz S, Wietrzynski W, Ohnishi N, Niemeyer J, Spaniol B, Schaffer M, Rast A, Ostermeier M, Strauss M, Plitzko JM, Baumeister W, Rudack T, Sakamoto W, Nickelsen J, Schuller JM, Schroda M, Engel BD (2021) Structural basis for VIPP1 oligomerization and maintenance of thylakoid membrane integrity. Cell 184(14):3643-3659.e3623. https://doi.org/10.1016/j.cell.2021.05.011
Heslopharrison J (1963a) Structure and morphogenesis of lamellar systems in grana-containing chloroplasts. Planta 60:243–260
Heslopharrison J (1963) Structure and morphogenesis of lamellar systems in grana-containing chloroplasts: 1. membrane structure and lamellar architecture. Planta 60(3):243–260. https://doi.org/10.1007/Bf01937960
Hinnah SC, Wagner R (1998) Thylakoid membranes contain a high-conductance channel. Eur J Biochem 253(3):606–613
Junge W, Witt HT (1968) On ion transport system of photosynthesis—investigations on a molecular level. Z Naturforsch B 23(2):244
Kadirjan-Kalbach DK, Turmo A, Wang J, Smith BC, Chen C, Porter KJ, Childs KL, DellaPenna D, Osteryoung KW (2019) Allelic Variation in the chloroplast division gene FtsZ2-2 leads to natural variation in chloroplast size. Plant Physiol 181(3):1059–1074. https://doi.org/10.1104/pp.19.00841
Karamoko M, El-Kafafi ES, Mandaron P, Lerbs-Mache S, Falconet D (2011) Multiple FtsZ2 isoforms involved in chloroplast division and biogenesis are developmentally associated with thylakoid membranes in Arabidopsis. FEBS Lett 585(8):1203–1208. https://doi.org/10.1016/j.febslet.2011.03.041
Kirchhoff H, Hall C, Wood M, Herbstova M, Tsabari O, Nevo R, Charuvi D, Shimoni E, Reich Z (2011) Dynamic control of protein diffusion within the granal thylakoid lumen. Proc Natl Acad Sci U S A 108(50):20248–20253. https://doi.org/10.1073/pnas.1104141109
Kroll D, Meierhoff K, Bechtold N, Kinoshita M, Westphal S, Vothknecht UC, Soll J, Westhoff P (2001) VIPP1, a nuclear gene of Arabidopsis thaliana essential for thylakoid membrane formation. Proc Natl Acad Sci U S A 98(7):4238–4242
Kulandaivelu G, Gnanam A (1985) Scanning electron-microscopic evidence for a budding mode of chloroplast multiplication in higher-plants. Physiol Plantarum 63(3):299–302. https://doi.org/10.1111/j.1399-3054.1985.tb04269.x
Leech RM, Thomson WW, Plattaloia KA (1981) Observations on the mechanism of chloroplast division in higher-plants. New Phytol 87(1):1–000. https://doi.org/10.1111/j.1469-8137.1981.tb01686.x
Li M, Mukhopadhyay R, Svoboda V, Oung HMO, Mullendore DL, Kirchhoff H (2020) Measuring the dynamic response of the thylakoid architecture in plant leaves by electron microscopy. Plant Direct 4(11):e00280. https://doi.org/10.1002/pld3.280
Lo SM, Theg SM (2012) Role of vesicle-inducing protein in plastids 1 in cpTat transport at the thylakoid. Plant J. https://doi.org/10.1111/j.1365-313X.2012.05020.x
Maple-Grodem J, Raynaud C (2014) Plastid division. In: Theg SM, Wollman FA (eds) Plastid biology. advances in plant biology, vol 5. Springer, New York, pp 155–188
McAndrew RS, Froehlich JE, Vitha S, Stokes KD, Osteryoung KW (2001) Colocalization of plastid division proteins in the chloroplast stromal compartment establishes a new functional relationship between FtsZ1 and FtsZ2 in higher plants. Plant Physiol 127(4):1656–1666. https://doi.org/10.1104/Pp.010542
Mercer FV, Hodge AJ, Hope AB, Mclean JD (1954) The structure and swelling properties of nitella chloroplasts. Aust J Biol Sci 8(1):1–18
Miyagishima SY, Froehlich JE, Osteryoung KW (2006) PDV1 and PDV2 mediate recruitment of the dynamin-related protein ARC5 to the plastid division site. Plant Cell 18(10):2517–2530. https://doi.org/10.1105/tpc.106.045484
Mustardy L, Buttle K, Steinbach G, Garab G (2008) The three-dimensional network of the thylakoid membranes in plants: quasihelical model of the granum-stroma assembly. Plant Cell 20(10):2552–2557. https://doi.org/10.1105/tpc.108.059147
Mustardy LA, Janossy AGS (1979) Evidence of helical thylakoid arrangement by scanning electron microscopy. Plant Sci Lett 16:281–284
Nierzwicki-Bauer SA, Balkwill DL, Stevens SE Jr (1983) Three-dimensional ultrastructure of a unicellular cyanobacterium. J Cell Biol 97(3):713–722
Nishio JN, Whitmarsh J (1991) Dissipation of the proton electrochemical potential in intact and lysed chloroplasts .1. the electrical potential. Plant Physiol 95(2):522–528. https://doi.org/10.1104/Pp.95.2.522
Oross JW, Possingham JV (1989) Ultrastructural features of the constricted region of dividing plastids. Protoplasma 150(2–3):131–138. https://doi.org/10.1007/Bf01403669
Paolillo D, Falk R (1966) The ultrastructure of grana in mesolhyll plastids of Zea mays. Am J Botany 53:173–180
Porter KJ, Cao L, Chen Y, TerBush AD, Chen C, Erickson HP, Osteryoung KW (2021) The Arabidopsis thaliana chloroplast division protein FtsZ1 counterbalances FtsZ2 filament stability in vitro. J Biol Chem 296:100627. https://doi.org/10.1016/j.jbc.2021.100627
Pyke KA, Leech RM (1994) A genetic-analysis of chloroplast division and expansion in Arabidopsis-thaliana. Plant Physiol 104(1):201–207
Pyke KA, Rutherford SM, Robertson EJ, Leech RM (1994) Arc6, a fertile Arabidopsis mutant with only 2 mesophyll cell chloroplasts. Plant Physiol 106(3):1169–1177
Robertson EJ, Pyke KA, Leech RM (1995) Arc6, an extreme chloroplast division mutant of arabidopsis also alters proplastid proliferation and morphology in shoot and root apices. J Cell Sci 108:2937–2944
Robertson EJ, Rutherford SM, Leech RM (1996) Characterization of chloroplast division using the Arabidopsis mutant arc5. Plant Physiol 112(1):149–159. https://doi.org/10.1104/Pp.112.1.149
Schonknecht G, Althoff G, Junge W (1990) The electric unit size of thylakoid membranes. FEBS Lett 277(1–2):65–68. https://doi.org/10.1016/0014-5793(90)80810-6
Shimoni E, Rav-Hon O, Ohad I, Brumfeld V, Reich Z (2005) Three-dimensional organization of higher-plant chloroplast thylakoid membranes revealed by electron tomography. Plant Cell 17(9):2580–2586. https://doi.org/10.1105/tpc.105.035030
Theg SM, Tom C (2011) Measurement of the DeltapH and electric field developed across Arabidopsis thylakoids in the light. Methods Mol Biol 775:327–341. https://doi.org/10.1007/978-1-61779-237-3_18
van Roon H, van Breemen JFL, de Weerd FL, Dekker JP, Boekema EJ (2000) Solubilization of green plant thylakoid membranes with n-dodecyl-alpha, D-maltoside. Implications for the structural organization of the photosystem II, photosystem I, ATP synthase and cytochrome b(6)f complexes. Photosynth Res 64(2–3):155–166. https://doi.org/10.1023/A:1006476213540
Vitha S, Froehlich JE, Koksharova O, Pyke KA, van Erp H, Osteryoung KW (2003) ARC6 is a J-domain plastid division protein and an evolutionary descendant of the cyanobacterial cell division protein Ftn2. Plant Cell 15(8):1918–1933
Wang Q, Sullivan RW, Kight A, Henry RL, Huang JR, Jones AM, Korth KL (2004) Deletion of the chloroplast-localized Thylakoid formation1 gene product in Arabidopsis leads to deficient thylakoid formation and variegated leaves. Plant Physiol 136(3):3594–3604. https://doi.org/10.1104/pp.104.049841
Weier TE, Stocking CR, Bracker CE, Risley EB (1965) Structural relationships of internal membrane systems of in situ and isolated chloroplasts of hordeum vulgare. Am J Bot 52(4):339. https://doi.org/10.2307/2440328
Whatley JM (1980) Plastid growth and division in phaseolus-vulgaris. New Phytol 86(1):1. https://doi.org/10.1111/j.1469-8137.1980.tb00774.x
Wietrzynski W, Schaffer M, Tegunov D, Albert S, Kanazawa A, Plitzko JM, Baumeister W, Engel BD (2020) Charting the native architecture of chlamydomonas thylakoid membranes with single-molecule precision. Elife. https://doi.org/10.7554/eLife.53740
Witt HT (1979) Energy-conversion in the functional membrane of photosynthesis—analysis by light-pulse and electric pulse methods—central role of the electric-field. Biochim Biophys Acta 505(3–4):355–427. https://doi.org/10.1016/0304-4173(79)90008-9
Yoshida Y (2018) Insights into the mechanisms of chloroplast division. Int J Mol Sci. 19(3):733. https://doi.org/10.3390/ijms19030733
Yoshida Y, Kuroiwa H, Misumi O, Nishida K, Yagisawa F, Fujiwara T, Nanamiya H, Kawamura F, Kuroiwa T (2006) Isolated chloroplast division machinery can actively constrict after stretching. Science 313(5792):1435–1438. https://doi.org/10.1126/science.1129689
Zhang M, Schmitz AJ, Kadirjan-Kalbach DK, Terbush AD, Osteryoung KW (2013) Chloroplast division protein ARC3 regulates chloroplast FtsZ-ring assembly and positioning in arabidopsis through interaction with FtsZ2. Plant Cell 25(5):1787–1802. https://doi.org/10.1105/tpc.113.111047
Acknowledgements
We would like to thank Dr. Katherine W. Osteryoung for providing us with arc6, pdv1-1, pdv1-2, pdv2-1, and pdv2-2 Arabidopsis seeds, Drs. Bo Liu and Yuh-Ru Julie Lee for providing access to their phase contrast microscope and for sharing their expertise in confocal microscopy. We would also like to thank Drs. Lan-Xin Shi and Li Liu for their expertise in plant tissue culture. This work was funded by the Division of Chemical Sciences, Geosciences, and Biosciences, Office of Basic Energy Sciences of the US Department of Energy through Grant DE-FG02-03ER15405.
Funding
This work was funded by the Division of Chemical Sciences, Geosciences, and Biosciences, Office of Basic Energy Sciences of the US Department of Energy through Grant DE-FG02-03ER15405.
Author information
Authors and Affiliations
Contributions
JH and SMT: designed experiments. JH, WK and VL: performed the experiments and all authors analyzed the data. JH and SMT: wrote the article and all authors approved it.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Ho, J., Kwan, W., Li, V. et al. Characterization of thylakoid division using chloroplast dividing mutants in Arabidopsis. Photosynth Res 157, 1–11 (2023). https://doi.org/10.1007/s11120-023-01002-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11120-023-01002-4