Diel leaf growth of soybean: a novel method to analyze two-dimensional leaf expansion in high temporal resolution based on a marker tracking approach (Martrack Leaf)

Plant Methods

Achim Walter¹  Norbert Kirchgessner¹  Michael Friedli¹  Michael Mielewczik¹ 

[1] ETH Zürich, Institute of Agricultural Sciences, Universitätstr. 2, CH-8092 Zürich, Switzerland

关键词: Natural illumination;    Diel growth;    Plant growth;    Image analysis;    Phenotyping;    Marker tracking;   

Others  :  820260
DOI  :  10.1186/1746-4811-9-30

 received in 2013-05-14, accepted in 2013-07-12,  发布年份 2013

【 摘 要 】

Background

We present a novel method for quantitative analysis of dicot leaf expansion at high temporal resolution. Image sequences of growing leaves were assessed using a marker tracking algorithm. An important feature of the method is the attachment of dark beads that serve as artificial landmarks to the leaf margin. The beads are mechanically constricted to the focal plane of a camera. Leaf expansion is approximated by the increase in area of the polygon defined by the centers of mass of the beads surrounding the leaf. Fluctuating illumination conditions often pose serious problems for tracking natural structures of a leaf; this problem is circumvented here by the use of the beads.

Results

The new method has been used to assess leaf growth in environmental situations with different illumination conditions that are typical in agricultural and biological experiments: Constant illumination via fluorescent light tubes in a climate chamber, a mix of natural and artificial illumination in a greenhouse and natural illumination of the situation on typical summer days in the field. Typical features of diel (24h) soybean leaf growth patterns were revealed in all three conditions, thereby demonstrating the general applicability of the method. Algorithms are provided to the entire community interested in using such approaches.

Conclusions

The implementation Martrack Leaf presented here is a robust method to investigate diel leaf growth rhythms both under natural and artificial illumination conditions. It will be beneficial for the further elucidation of genotype x environment x management interactions affecting leaf growth processes.

【 授权许可】

   
2013 Mielewczik et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Figure 7.

Figure 8.

【 参考文献 】

• [1]McClung CR: Circadian rhythms in plants. Annual Review of Plant Biology 2001, 52:139-162.
• [2]Poiré R, Wiese-Klinkenberg A, Parent B, Mielewczik M, Schurr U, Tardieu F, Walter A: Diel time-courses of leaf growth in monocot and dicot species: endogenous rhythms and temperature effects. Journal of Experimental Botany 2010, 61:1751-1759.
• [3]Dodd AN, Salathia N, Hall A, Kévei E, Tóth R, Nagy F, Hibberd JM, Millar AJ, Webb AA: Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science Signaling 2005, 309:630.
• [4]Kinmonth-Schultz HA, Golembeski GS, Imaizumi T: Circadian clock-regulated physiological outputs: dynamic responses in nature. In Seminars in Cell & Developmental Biology: Elsevier; 2013.
• [5]Lu Y, Gehan JP, Sharkey TD: Daylength and circadian effects on starch degradation and maltose metabolism. Plant Physiology 2005, 138:2280-2291.
• [6]Hennessey TL, Field CB: Circadian rhythms in photosynthesis oscillations in carbon assimilation and stomatal conductance under constant conditions. Plant Physiology 1991, 96:831-836.
• [7]Espinoza C, Degenkolbe T, Caldana C, Zuther E, Leisse A, Willmitzer L, Hincha DK, Hannah MA: Interaction with diurnal and circadian regulation results in dynamic metabolic and transcriptional changes during cold acclimation in Arabidopsis. PloS One 2010, 5:e14101.
• [8]Dodd AN, Kusakina J, Hall A, Gould PD, Hanaoka M: The circadian regulation of photosynthesis. Photosynthesis research 2013, 1-10.
• [9]Nozue K, Covington MF, Duek PD, Lorrain S, Fankhauser C, Harmer SL, Maloof JN: Rhythmic growth explained by coincidence between internal and external cues. Nature 2007, 448:358-361.
• [10]Graf A, Schlereth A, Stitt M, Smith AM: Circadian control of carbohydrate availability for growth in Arabidopsis plants at night. Proceedings of the National Academy of Sciences 2010, 107:9458-9463.
• [11]Graf A, Smith AM: Starch and the clock: the dark side of plant productivity. Trends in Plant Science 2011, 16:169-175.
• [12]Farré E: The regulation of plant growth by the circadian clock. Plant Biology 2012, 14:401-410.
• [13]Millar AJ: Input signals to the plant circadian clock. Journal of Experimental Botany 2004, 55:277-283.
• [14]McClung CR, Gutiérrez RA: Network news: prime time for systems biology of the plant circadian clock. Current Opinion in Genetics & Development 2010, 20:588-598.
• [15]Horiguchi G, Ferjani A, Fujikura U, Tsukaya H: Coordination of cell proliferation and cell expansion in the control of leaf size in Arabidopsis thaliana. Journal of Plant Research 2006, 119:37-42.
• [16]Horiguchi G, Fujikura U, Ferjani A, Ishikawa N, Tsukaya H: Large‒scale histological analysis of leaf mutants using two simple leaf observation methods: identification of novel genetic pathways governing the size and shape of leaves. The Plant Journal 2006, 48:638-644.
• [17]Walter A, Schurr U: Dynamics of leaf and root growth: endogenous control versus environmental impact. Annals of Botany 2005, 95:891-900.
• [18]Walter A, Christ MM, Rascher U, Schurr U, Osmond B: Diel leaf growth cycles in Clusia spp. are related to changes between C3 photosynthesis and crassulacean acid metabolism during development and during water stress. Plant, Cell & Environment 2008, 31:484-491.
• [19]Poiré R, Schneider H, Thorpe MR, Kuhn AJ, Schurr U, Walter A: Root cooling strongly affects diel leaf growth dynamics, water and carbohydrate relations in Ricinus communis. Plant, Cell & Environment 2010, 33:408-417.
• [20]Kjaer KH, Poiré R, Ottosen C-O, Walter A: Rapid adjustment in chrysanthemum carbohydrate turnover and growth activity to a change in time-of-day application of light and daylength. Functional Plant Biology 2012, 39:639-649.
• [21]Ruts T, Matsubara S, Wiese-Klinkenberg A, Walter A: Diel patterns of leaf and root growth: endogenous rhythmicity or environmental response? Journal of Experimental Botany 2012, 63:3339-3351.
• [22]Roden J, Van Volkenburgh E, Hinckley T: Cellular basis for limitation of poplar leaf growth by water deficit. Tree Physiology 1990, 6:211-219.
• [23]Taylor G, Davies W: The control of leaf growth of Betula and Acer by photoenvironment. New Phytologist 1985, 101:259-268.
• [24]Takami SC, Rawson HM, Turner NC: Leaf expansion of four sunflower (Helianthus annuus L.) cultivars in relation to water deficits. II. Diurnal patterns during stress and recovery. Plant, Cell & Environment 1982, 5:279-286.
• [25]Reymond M, Muller B, Leonardi A, Charcosset A, Tardieu F: Combining quantitative trait loci analysis and an ecophysiological model to analyze the genetic variability of the responses of maize leaf growth to temperature and water deficit. Plant Physiology 2003, 131:664-675.
• [26]Munns R, Passioura JB, Guo J, Chazen O, Cramer GR: Water relations and leaf expansion: importance of time scale. Journal of Experimental Botany 2000, 51:1495-1504.
• [27]Wilhelm W, Nelson C: Leaf growth, leaf aging, and photosynthetic rate of tall fescue genotypes. Publications from USDA-ARS/UNL Faculty 1978, Paper 126: . (http://digitalcommons.unl.edu/usdaarsfacpub/126 webcite) reprint from Crop Science 1978, 18:769-772
• [28]Timm S, Mielewczik M, Florian A, Frankenbach S, Dreissen A, Hocken N, Fernie AR, Walter A, Bauwe H: High-to-low CO2 acclimation reveals plasticity of the photorespiratory pathway and indicates regulatory links to cellular metabolism of Arabidopsis. PloS One 2012, 7:e42809.
• [29]Wiese A, Christ M, Virnich O, Schurr U, Walter A: Spatio‒temporal leaf growth patterns of Arabidopsis thaliana and evidence for sugar control of the diel leaf growth cycle. New Phytologist 2007, 174:752-761.
• [30]Schmundt D, Stitt M, Jähne B, Schurr U: Quantitative analysis of the local rates of growth of dicot leaves at a high temporal and spatial resolution, using image sequence analysis. The Plant Journal 1998, 16:505-514.
• [31]Van Der Weele CM, Jiang HS, Palaniappan KK, Ivanov VB, Palaniappan K, Baskin TI: A new algorithm for computational image analysis of deformable motion at high spatial and temporal resolution applied to root growth. Roughly uniform elongation in the meristem and also, after an abrupt acceleration, in the elongation zone. Plant Physiology 2003, 132:1138-1148.
• [32]Walter A, Silk WK, Schurr U: Environmental effects on spatial and temporal patterns of leaf and root growth. Annual Review of Plant Biology 2009, 60:279-304.
• [33]Ruge U, Whaley WG, Ziegler H: Methoden der Wachstumsmessung. In Growth and Growth Substances/Wachstum und Wuchsstoffe. Springer; 1961:47-173.
• [34]Gallagher J, Biscoe P, Saffell R: A sensitive auxanometer for field use. Journal of experimental botany 1976, 27:704-716.
• [35]Körner C, Woodward F: The dynamics of leaf extension in plants with diverse altitudinal ranges. Oecologia 1987, 72:279-283.
• [36]Avery GS: Structure and development of tobacco leaves. American Journal of Botany 1933, 20:565-592.
• [37]Walter A, Schurr U: The modular character of growth in Nicotiana tabacum plants under steady state nutrition. Journal of Experimental Botany 1999, 50:1169-1177.
• [38]Walter A, Scharr H, Gilmer F, Zierer R, Nagel KA, Ernst M, Wiese A, Virnich O, Christ MM, Uhlig B, Jünger S, Schurr U: Dynamics of seedling growth acclimation towards altered light conditions can be quantified via GROWSCREEN: a setup and procedure designed for rapid optical phenotyping of different plant species. New Phytologist 2007, 174:447-455.
• [39]Granier C, Aguirrezabal L, Chenu K, Cookson SJ, Dauzat M, Hamard P, Thioux JJ, Rolland G, Bouchier‒Combaud S, Lebaudy A, Muller B, Simonneau T, Tardieu F: PHENOPSIS, an automated platform for reproducible phenotyping of plant responses to soil water deficit in Arabidopsis thaliana permitted the identification of an accession with low sensitivity to soil water deficit. New Phytologist 2006, 169:623-635.
• [40]Jansen M, Gilmer F, Biskup B, Nagel KA, Rascher U, Fischbach A, Briem S, Dreissen G, Tittmann S, Braun S, de Jaeger I, Metzlaff M, Schurr U, Scharr H, Walter A: Simultaneous phenotyping of leaf growth and chlorophyll fluorescence via GROWSCREEN FLUORO allows detection of stress tolerance in Arabidopsis thaliana and other rosette plants. Functional Plant Biology 2009, 36:902-914.
• [41]De Vylder J, Vandenbussche F, Hu Y, Philips W, Van Der Straeten D: Rosette Tracker: an open source image analysis tool for automatic quantification of genotype effects. Plant Physiology 2012, 160:1149-1159.
• [42]Arvidsson S, Pérez‒Rodríguez P, Mueller‒Roeber B: A growth phenotyping pipeline for Arabidopsis thaliana integrating image analysis and rosette area modeling for robust quantification of genotype effects. New Phytologist 2011, 191:895-907.
• [43]Leister D, Varotto C, Pesaresi P, Niwergall A, Salamini F: Large-scale evaluation of plant growth in Arabidopsis thaliana by non-invasive image analysis. Plant Physiology and Biochemistry 1999, 37:671-678.
• [44]Taylor G, Tricker PJ, Zhang FZ, Alston VJ, Miglietta F, Kuzminsky E: Spatial and temporal effects of free-air CO2 enrichment (POPFACE) on leaf growth, cell expansion, and cell production in a closed canopy of poplar. Plant Physiology 2003, 131:177-185.
• [45]Matsubara S, Hurry V, Druart N, Benedict C, Janzik I, Chavarría-Krauser A, Walter A, Schurr U: Nocturnal changes in leaf growth of Populus deltoides are controlled by cytoplasmic growth. Planta 2006, 223:1315-1328.
• [46]Matsubara S, Walter A: Living in day-night cycles–specific diel leaf growth patterns and the circadian control of photomorphogenesis. In Progress in Botany. Springer; 2007:288-314.
• [47]Nagel KA, Kastenholz B, Jahnke S, van Dusschoten D, Aach T, Mühlich M, Truhn D, Scharr H, Terjung S, Walter A: Temperature responses of roots: impact on growth, root system architecture and implications for phenotyping. Functional Plant Biology 2009, 36:947-959.
• [48]Walter A, Spies H, Terjung S, Küsters R, Kirchgeßner N, Schurr U: Spatio‒temporal dynamics of expansion growth in roots: automatic quantification of diurnal course and temperature response by digital image sequence processing. Journal of Experimental Botany 2002, 53:689-698.
• [49]Walter A, Feil R, Schurr U: Expansion dynamics, metabolite composition and substance transfer of the primary root growth zone of Zea mays L. grown in different external nutrient availabilities. Plant, Cell & Environment 2003, 26:1451-1466.
• [50]Bergougnoux V, Zalabák D, Jandová M, Novák O, Wiese-Klinkenberg A, Fellner M: Effect of blue light on endogenous isopentenyladenine and endoreduplication during photomorphogenesis and de-etiolation of tomato (Solanum lycopersicum L.) seedlings. PloS One 2012, 7:e45255.
• [51]Schurr U, Walter A, Terjung S, Spies H, Kirchgessner N, Scharr H, Küsters R: Dynamics of leaf and root growth. Science Access 2001, 3: .
• [52]Ruts T, Matsubara S, Wiese‒Klinkenberg A, Walter A: Aberrant temporal growth pattern and morphology of root and shoot caused by a defective circadian clock in Arabidopsis thaliana. The Plant Journal 2012, 72:154-161.
• [53]Spies H, Kirchgeßner N, Scharr H, Jähne B: Dense structure estimation via regularised optical flow. In VMV 2000; Berlin Akad. Verl.-Ges. Aka. Amsterdam: Ios Press; 2000:57-64.
• [54]Schuchert T, Scharr H: An affine optical flow model for dynamic surface reconstruction. In Statistical and Geometrical Approaches to Visual Motion Analysis. Springer; 2009:70-90.
• [55]Haussecker HW, Fleet DJ: Computing optical flow with physical models of brightness variation. In Proceedings IEEE Conference on Computer Vision and Pattern Recognition. Hilton Head Island, South Carolina June 13-15. Los Alamitos, California, Washington, Brussels, Tokyo: IEEE Computer Society; 2000, Volume II:760-767.
• [56]Horn BK, Schunck BG: Determining optical flow. Artificial intelligence 1981, 17:185-203.
• [57]Schurr U: Growth physiology: approaches to a spatially and temporarily varying problem. In Progress in Botany. Springer; 1998:355-373.
• [58]Beemster GT, Baskin TI: Analysis of cell division and elongation underlying the developmental acceleration of root growth in Arabidopsis thaliana. Plant Physiology 1998, 116:1515-1526.
• [59]Basu P, Pal A, Lynch JP, Brown KM: A novel image-analysis technique for kinematic study of growth and curvature. Plant Physiology 2007, 145:305-316.
• [60]Ishikawa H, Evans M: Novel software for analysis of root gravitropism: comparative response patterns of Arabidopsis wild‒type and axr1 seedlings. Plant, Cell & Environment 1997, 20:919-928.
• [61]Remmler L, Rolland-Lagan A-G: Computational method for quantifying growth patterns at the adaxial leaf surface in three dimensions. Plant Physiology 2012, 159:27-39.
• [62]Wang L, Beyer ST, Cronk QC, Walus K: Delivering high-resolution landmarks using inkjet micropatterning for spatial monitoring of leaf expansion. Plant Methods 2011, 7:1. BioMed Central Full Text
• [63]Lewis J: Fast normalized cross-correlation. Vision interface 1995, 120-123.
• [64]Tian Q, Huhns MN: Algorithms for subpixel registration. Computer Vision, Graphics, and Image Processing 1986, 35:220-233.
• [65]Ainsworth EA, Walter A, Schurr U: Glycine max leaflets lack a base-tip gradient in growth rate. Journal of Plant Research 2005, 118:343-346.
• [66]Wei S-D, Pan W-H, Lai S-H: A novel motion estimation method based on normalized cross correlation for video compression. In Advances in Multimedia Modeling. Springer; 2008:338-347.
• [67]Huang Y-W, Chen C-Y, Tsai C-H, Shen C-F, Chen L-G: Survey on block matching motion estimation algorithms and architectures with new results. Journal of VLSI signal processing systems for signal, image and video technology 2006, 42:297-320.
• [68]Barjatya A: Block matching algorithms for motion estimation. IEEE Transactions Evolution Computation 2004, 8:225-239.
• [69]Cesa CM, Kirchgessner N, Mayer D, Schwarz US, Hoffmann B, Merkel R: Micropatterned silicone elastomer substrates for high resolution analysis of cellular force patterns. Review of Scientific Instruments 2007, 78:034301-034310.