, Volume 223, Issue 6, pp 1315–1328

Nocturnal changes in leaf growth of Populus deltoides are controlled by cytoplasmic growth

  • Shizue Matsubara
  • Vaughan Hurry
  • Nathalie Druart
  • Catherine Benedict
  • Ingar Janzik
  • Andrés Chavarría-Krauser
  • Achim Walter
  • Ulrich Schurr
Original Article


Growing leaves do not expand at a constant rate but exhibit pronounced diel growth rhythms. However, the mechanisms giving rise to distinct diel growth dynamics in different species are still largely unknown. As a first step towards identifying genes controlling rate and timing of leaf growth, we analysed the transcriptomes of rapidly expanding and fully expanded leaves of Populus deltoides Bartr. ex. Marsh at points of high and low expansion at night. Tissues with well defined temporal growth rates were harvested using an online growth-monitoring system based on a digital image sequence processing method developed for quantitative mapping of dicot leaf growth. Unlike plants studied previously, leaf growth in P. deltoides was characterised by lack of a base-tip gradient across the lamina, and by maximal and minimal growth at dusk and dawn, respectively. Microarray analysis revealed that the nocturnal decline in growth coincided with a concerted down-regulation of ribosomal protein genes, indicating deceleration of cytoplasmic growth. In a subsequent time-course experiment, Northern blotting and real-time RT-PCR confirmed that the ribosomal protein gene RPL12 and a cell-cycle gene H2B were down-regulated after midnight following a decrease in cellular carbohydrate concentrations. Thus, we propose that the spatio-temporal growth pattern in leaves of P. deltoides primarily arises from cytoplasmic growth whose activity increases from afternoon to midnight and thereafter decreases in this species.


Cell cycle Cytoplasmic growth Leaf growth Microarray Populus Ribosomal protein 



Leaf plastochron index


Mature leaves


Relative growth rate


Ribosomal protein


Young leaves


  1. Beemster GTS, De Veylder L, Vercruysse S, West G, Rombaut D, Van Hummelen P, Galichet A, Gruissem W, Inzé D, Vuylsteke M (2005) Genome-wide analysis of gene expression profiles associated with cell cycle transitions in growing organs of Arabidopsis. Plant Physiol 138:734–743PubMedCrossRefGoogle Scholar
  2. Bertram L, Lercari B (1997) Kinetics of stem elongation in light-grown tomato plants. Responses to different photosynthetically active radiation levels by wild-type and aurea mutant plants. Photochem Photobiol 66:396–403CrossRefGoogle Scholar
  3. Bhalerao R, Nilsson O, Sandberg G (2003) Out of the woods: forest biotechnology enters the genomic era. Curr Opin Biotechnol 14:206–213PubMedCrossRefGoogle Scholar
  4. Bigün J, Granlund GH (1987) Optimal orientation detection of linear symmetry. In: Proceedings of the 1st international conference on computer vision (ICCV). London, UKGoogle Scholar
  5. Bolige A, Hagiwara S, Zhang Y, Goto K (2005) Circadian G2 arrest as related to circadian gating of cell proliferation growth in Euglena. Plant Cell Physiol 46:931–936PubMedCrossRefGoogle Scholar
  6. Breyne P, Dreesen R, Vandepoele K, De Veylder L, Van Breusegem F, Callewaert L, Rombauts S, Raes J, Cannoot B, Engler G, Inzé D, Zabeau M (2002) Transcriptome analysis during cell division in plants. Proc Natl Acad Sci USA 99:14825–14830PubMedCrossRefGoogle Scholar
  7. Britt AB (1996) DNA damage and repair in plants. Annu Rev Plant Physiol Plant Mol Biol 4:75–100CrossRefGoogle Scholar
  8. Brunner AM, Busov VB, Strauss SH (2004) Poplar genome sequence: functional genomics in an ecologically dominant plant species. Trends Plant Sci 9:49–56PubMedCrossRefGoogle Scholar
  9. Bünning E (1952) Über den Tagesrhythmus der Mitosehäufigkeit in Pflanzen. Z Bot 40:193–199Google Scholar
  10. Chang SJ, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Reporter 11:113–116CrossRefGoogle Scholar
  11. Christ RA (1978) The elongation rate of wheat leaves. J Exp Bot 29:611–618CrossRefGoogle Scholar
  12. Cosgrove DJ (2000) Expansive growth of plant cell walls. Plant Physiol Biochem 38:109–124PubMedCrossRefGoogle Scholar
  13. Cronk QCB (2005) Plant eco-devo: the potential of poplar as a model organism. New Phytol 166:39–48PubMedCrossRefGoogle Scholar
  14. Cuadrado A, Navarrete MH, Canovas JL (1985) The effect of partial protein synthesis inhibition on cell proliferation in higher plants. J Cell Sci 76:97–104PubMedGoogle Scholar
  15. Dale JE (1988) The control of leaf expansion. Ann Rev Plant Physiol Plant Mol Biol 39:267–295CrossRefGoogle Scholar
  16. den Boer BGW, Murray JAH (2000) Triggering the cell cycle in plants. Trends Cell Biol 10:245–250CrossRefGoogle Scholar
  17. Diaz E, Yang Y, Ferreira T, Loh K, Okazaki Y, Hayashizaki Y, Tessier-Lavigne M, Speed T, Ngai J (2003) Analysis of gene expression in the developing mouse retina. Proc Natl Acad Sci USA 100:5491–5496PubMedCrossRefGoogle Scholar
  18. Dodd AN, Salathia N, Hall A, Kévei E, Tóth R, Nagy F, Hibberd JM, Millar AJ, Webb AAR (2005) Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309:630–633PubMedCrossRefGoogle Scholar
  19. Donnelly PM, Bonetta D, Tsukaya H, Dengler RE, Dengler NG (1999) Cell cycling and cell enlargement in developing leaves of Arabidopsis. Dev Biol 215:407–419PubMedCrossRefGoogle Scholar
  20. Edwards D (2003) Non-linear normalization and background correction in one-channel cDNA microarray studies. Bioinformatics 19:825–833PubMedCrossRefGoogle Scholar
  21. Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95:14863–14868PubMedCrossRefGoogle Scholar
  22. Erickson RO, Michelini FJ (1957) The plastochron index. Am J Bot 44:297–305CrossRefGoogle Scholar
  23. Goto K, Johnson CH (1995) Is the cell division cycle gated by a circadian clock? The case of Chlamydomonas reinhardtii. J Cell Biol 129:1061–1069PubMedCrossRefGoogle Scholar
  24. Granier C, Tardieu F (1998) Spatial and temporal analyses of expansion and cell cycle in sunflower leaves. Plant Physiol 116:991–1001PubMedCrossRefGoogle Scholar
  25. Harmer SL, Hogenesch JB, Straume M, Chang H-S, Han B, Zhu T, Wang X, Kreps JA, Kay SA (2000) Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290:2110–2113PubMedCrossRefGoogle Scholar
  26. Hayama R, Coupland G (2003) Shedding light on the circadian clock and the photoperiodic control of flowering. Curr Opin Plant Biol 6:13–19PubMedCrossRefGoogle Scholar
  27. Ito T, Kim G-T, Shinozaki K (2000) Disruption of an Arabidopsis cytoplasmic ribosomal protein S13-homologous gene by transposon-mediated mutagenesis causes aberrant growth and development. Plant J 22:257–264PubMedCrossRefGoogle Scholar
  28. Jorgensen P, Tyers M, Warner JR (2004) Forging the factory: ribosome synthesis and growth control in budding yeast. In: Hall MN, Raff M, Thomas G (eds) Cell growth: control of cell size. Cold Spring Harbor Laboratory Press, New York, pp 329–370Google Scholar
  29. Kohler A, Blaudez D, Chalot M, Martin F (2004) Cloning and expression of multiple metallothioneins from hybrid poplar. New Phytol 164:83–93CrossRefGoogle Scholar
  30. Krause GH, Gallé A, Gademann R, Winter K (2003) Capacity of protection against ultraviolet radiation in sun and shade leaves of tropical forest plants. Funct Plant Biol 30:533–542CrossRefGoogle Scholar
  31. Larson PR, Isebrands JG (1971) The plastochron index as applied to developmental studies of cottonwood. Can J For Res 1:1–11CrossRefGoogle Scholar
  32. Mayrhofer S, Heizmann U, Magel E, Eiblmeier M, Müller A, Rennenberg H, Hampp R, Schnitzler J-P, Kreuzwieser J (2004) Carbon balance in leaves of young poplar trees. Plant Biol 6:1–10CrossRefGoogle Scholar
  33. Menges M, Hennig L, Gruissem W, Murray JAH (2002) Cell cycle-regulated gene expression in Arabidopsis. J Biol Chem 277:41987–42002PubMedCrossRefGoogle Scholar
  34. Nakazono M, Qiu F, Borsuk LA, Schnable PS (2003) Laser-capture microdissection, a tool for the global analysis of gene expression in specific plant cell types: identification of genes expressed differentially in epidermal cells or vascular tissues of maize. Plant Cell 15:583–596PubMedCrossRefGoogle Scholar
  35. Nikaido SS, Johnson CH (2000) Daily and circadian variation in survival from ultraviolet radiation in Chlamydomonas reinhardtii. Photochem Photobiol 71:758–765PubMedCrossRefGoogle Scholar
  36. Poethig RS, Sussex IM (1985) The cellular parameters of leaf development in tobacco: a clonal analysis. Planta 165:170–184CrossRefGoogle Scholar
  37. Popescu SC, Tumer NE (2004) Silencing of ribosomal protein L3 genes in N. tabacum reveals coordinate expression and significant alterations in plant growth, development and ribosome biogenesis. Plant J 39:29–44PubMedCrossRefGoogle Scholar
  38. Roggatz U, McDonald AJS, Stadenberg I, Schurr U (1999) Effects of nitrogen deprivation on cell division and expansion in leaves of Ricinus communis L. Plant Cell Environ 22:81–89CrossRefGoogle Scholar
  39. Schaffer R, Landgraf J, Accerbi M, Simon V, Larson M, Wisman E (2001) Microarray analysis of diurnal and circadian-regulated genes in Arabidopsis. Plant Cell 13:113–123PubMedCrossRefGoogle Scholar
  40. Schaffer R, Ramsay N, Samach A, Corden S, Putterill J, Carré IA, Coupland G (1998) The late elongated hypocotyl mutation of Arabidopsis disrupts circadian rhythms and the photoperiodic control of flowering. Cell 93:1219–1229PubMedCrossRefGoogle Scholar
  41. Scharr H (2005) Optimal filters for extended optical flow. In: Proceedings of international workshop on complex motion. Günzburg, Germany, LNCS 3417Google Scholar
  42. Schawalder SB, Kabani M, Howald I, Choudhury U, Werner M, Shore D (2004) Growth-regulated recruitment of the essential yeast ribosomal protein gene activator lfh1. Nature 432:1058–1061PubMedCrossRefGoogle Scholar
  43. Schmundt D, Stitt M, Jähne B, Schurr U (1998) Quantitative analysis of the local rates of growth of dicot leaves at a high temporal and spatial resolution, using image sequence analysis. Plant J 16:505–514CrossRefGoogle Scholar
  44. Smith C, Rodríguez-Buey M, Karlsson J, Campbell MM (2004) The response of the poplar transcriptome to wounding and subsequent infection by a viral pathogen. New Phytol 164:123–136CrossRefGoogle Scholar
  45. Stahlberg R, Van Volkenburgh E (1999) The effect of light on membrane potential, apoplastic pH and cell expansion in leaves of Pisum sativum L. var. Argenteum. Planta 208:188–195CrossRefGoogle Scholar
  46. Stals H, Inzé D (2001) When plant cells decide to divide. Trends Plant Sci 6:359–364PubMedCrossRefGoogle Scholar
  47. Stapleton AE, Walbot V (1994) Flavonoids can protect maize DNA from the induction of ultraviolet-radiation damage. Plant Physiol 105:881–889PubMedCrossRefGoogle Scholar
  48. Sterky F, Bhalerao RR, Unneberg P, Segerman B, Nilsson P, Brunner AM, Charbonnel-Campaa L, Jonsson-Lindvall J, Tandre K, Strauss SH, Sundberg B, Gustafsson P, Uhlén M, Bhalerao RP, Nilsson O, Sandberg G, Karlsson J, Lundeberg J, Jansson S (2004) A Populus EST resource for plant functional genomics. Proc Natl Acad Sci USA 101:13951–13956PubMedCrossRefGoogle Scholar
  49. Stiles KA, Van Volkenburgh E (2002) Light-regulated leaf expansion in two Populus species: dependence on developmentally controlled ion transport. J Exp Bot 53:1651–1657PubMedCrossRefGoogle Scholar
  50. Sugimoto-Shirasu K, Roberts K (2003) “Big it up”: endoreduplication and cell-size control in plants. Curr Opin Plant Biol 6:544–553PubMedCrossRefGoogle Scholar
  51. Taylor G (2002) Populus: arabidopsis for forestry. Do we need a model tree? Ann Bot 90:681–689PubMedCrossRefGoogle Scholar
  52. Trainotti L, Pavanello A, Casadoro G (2004) Differential expression of genes in apical and basal tissues of expanding tobacco leaves. Plant Sci 167:679–686CrossRefGoogle Scholar
  53. Van der Werf A (1996) Growth analysis and photoassimilate partitioning. In: Zamski E, Schaffer AA (eds) Photoassimilate distribution in plants and crops. Marcel Dekker, New York, pp 1–20Google Scholar
  54. Van Lijsebettens M, Vanderhaeghen R, De Block M, Bauw G, Villarroel R, Van Montagu M (1994) An S18 ribosomal protein gene copy at the Arabidopsis PFL locus affects plant development by its specific expression in meristems. EMBO J 13:3378–3388PubMedGoogle Scholar
  55. Van Volkenburgh E, Taylor G (1996) Leaf growth physiology. In: Stettler RF, Bradshaw HDJr, Heilman PE, Hinckley TM (eds) Biology of populus. NRC Research Press, Ottawa, pp 283–299Google Scholar
  56. Walter A, Christ MM, Barron-Gafford GA, Grieve KA, Paige T, Murthy R, Rascher U (2005) The effect of elevated CO2 on diel leaf growth cycle, leaf carbohydrate content and canopy growth performance of Populus deltoides. Global Change Biol 11:1207–1219CrossRefGoogle Scholar
  57. Walter A, Schurr U (2005) Dynamics of leaf and root growth—endogenous control versus environmental impact. Ann Bot 95:891–900PubMedCrossRefGoogle Scholar
  58. Warner JR (1999) The economics of ribosome biosynthesis in yeast. Trends Biochem Sci 24:437–440PubMedCrossRefGoogle Scholar
  59. Weijers D, Franke-van Dijk M, Vencken R-J, Quint A, Hooykaas P, Offringa R (2001) An Arabidopsis minute-like phenotype caused by a semi-dominant mutation in a RIBOSOMAL PROTEIN S5 gene. Development 128:4289–4299PubMedGoogle Scholar
  60. Wettenhall JM, Smyth GK (2004) LimmaGUI: a graphical user interface for linear modeling of microarray data. Bioinformatics 20:3705–3706PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • Shizue Matsubara
    • 1
  • Vaughan Hurry
    • 2
  • Nathalie Druart
    • 3
  • Catherine Benedict
    • 2
  • Ingar Janzik
    • 1
  • Andrés Chavarría-Krauser
    • 1
  • Achim Walter
    • 1
  • Ulrich Schurr
    • 1
  1. 1.Institut for Chemistry and Dynamics of the Geosphere: Phytosphere (ICG-III)Research Centre JülichJülichGermany
  2. 2.Umeå Plant Science Centre, Department of Plant PhysiologyUmeå UniversityUmeåSweden
  3. 3.Umeå Plant Science Centre, Department of Forest Genetics and Plant PhysiologySwedish University of Agricultural SciencesUmeåSweden

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