Measuring the diurnal pattern of leaf hyponasty and growth in Arabidopsis – a novel phenotyping approach using laser scanning
Tino Dornbusch A C , Séverine Lorrain A , Dmitry Kuznetsov B , Arnaud Fortier B , Robin Liechti B , Ioannis Xenarios B and Christian Fankhauser A C
+ Author Affiliations
- Author Affiliations
A Center for Integrative Genomics, Faculty of Biology and Medicine, University of Lausanne, 1015 Lausanne, Switzerland.
B SIB-Swiss Institute of Bioinformatics, University of Lausanne, 1015 Lausanne, Switzerland.
C Corresponding authors. Email: christian.fankhauser@unil.ch; tino.dornbusch@unil.ch
Functional Plant Biology 39(11) 860-869 https://doi.org/10.1071/FP12018
Submitted: 20 January 2012 Accepted: 15 May 2012 Published: 1 August 2012
Abstract
Plants forming a rosette during their juvenile growth phase, such as Arabidopsis thaliana (L.) Heynh., are able to adjust the size, position and orientation of their leaves. These growth responses are under the control of the plants circadian clock and follow a characteristic diurnal rhythm. For instance, increased leaf elongation and hyponasty – defined here as the increase in leaf elevation angle – can be observed when plants are shaded. Shading can either be caused by a decrease in the fluence rate of photosynthetically active radiation (direct shade) or a decrease in the fluence rate of red compared with far-red radiation (neighbour detection). In this paper we report on a phenotyping approach based on laser scanning to measure the diurnal pattern of leaf hyponasty and increase in rosette size. In short days, leaves showed constitutively increased leaf elevation angles compared with long days, but the overall diurnal pattern and the magnitude of up and downward leaf movement was independent of daylength. Shade treatment led to elevated leaf angles during the first day of application, but did not affect the magnitude of up and downward leaf movement in the following day. Using our phenotyping device, individual plants can be non-invasively monitored during several days under different light conditions. Hence, it represents a proper tool to phenotype light- and circadian clock-mediated growth responses in order to better understand the underlying regulatory genetic network.
Additional keywords: Arabidopsis, circadian clock, diurnal, hyponasty, image processing, laser scanning, leaf elongation, petiole angle, phenotyping.
References
Boyes DC, Zayed AM, Ascenzi R, McCaskill AJ, Hoffman NE, Davis KR, Görlach J (2001) Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. The Plant Cell 13, 1499–1510.Cox MCH, Millenaar FF, de Jong van Berkel YEM, Peeters AJM, Voesenek LACJ (2003) Plant movement. Submergence-induced petiole elongation in Rumex palustris depends on hyponastic growth. Plant Physiology 132, 282–291.
| Plant movement. Submergence-induced petiole elongation in Rumex palustris depends on hyponastic growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXktVGgsb4%3D&md5=99121143c70c1ea173dd46748b0dad99CAS |
de Kroon H, Visser EJW, Huber H, Mommer L, Hutchings MJ (2009) A modular concept of plant foraging behaviour: the interplay between local responses and systemic control. Plant, Cell & Environment 32, 704–712.
| A modular concept of plant foraging behaviour: the interplay between local responses and systemic control.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmslemsLk%3D&md5=7a1a0bfa4af1639f7e61c56cf4c6d1a7CAS |
Dhondt S, Vanhaeren H, Van Loo D, Cnudde V, Inzé D (2010) Plant structure visualization by high-resolution x-ray computed tomography. Trends in Plant Science 15, 419–422.
| Plant structure visualization by high-resolution x-ray computed tomography.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpvV2isLY%3D&md5=c950e3dce0a8a3e25af27856e3efccc7CAS |
Dornbusch T, Wernecke P, Diepenbrock W (2007) A method to extract morphological traits of plant organs from 3D point clouds as a database for an architectural plant model. Ecological Modelling 200, 119–129.
| A method to extract morphological traits of plant organs from 3D point clouds as a database for an architectural plant model.Crossref | GoogleScholarGoogle Scholar |
Ehleringer JR (1988) Changes in leaf characteristics of species along elevational gradients in the Wasatch Front, Utah. American Journal of Botany 75, 680–689.
| Changes in leaf characteristics of species along elevational gradients in the Wasatch Front, Utah.Crossref | GoogleScholarGoogle Scholar |
Forseth IN, Teramura AH (1986) Kudzu leaf energy budget and calculated transpiration: the influence of leaflet orientation. Ecology 67, 564–571.
| Kudzu leaf energy budget and calculated transpiration: the influence of leaflet orientation.Crossref | GoogleScholarGoogle Scholar |
Ichihashi Y, Kawade K, Usami T, Horiguchi G, Takahashi T, Tsukaya H (2011) Key proliferative activity in the junction between the leaf blade and leaf petiole of Arabidopsis. Plant Physiology 157, 1151–1162.
| Key proliferative activity in the junction between the leaf blade and leaf petiole of Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFehur%2FO&md5=f8f7161f97172c84274b927a013b35f7CAS |
Kaminuma E, Heida N, Tsumoto Y, Yamamoto N, Goto N, Okamoto N, Konagaya A, Matsui M, Toyoda T (2004) Automatic quantification of morphological traits via three-dimensional measurement of Arabidopsis. The Plant Journal 38, 358–365.
| Automatic quantification of morphological traits via three-dimensional measurement of Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Kaminuma E, Yoshizumi T, Wada T, Matsui M, Toyoda T (2008) Quantitative analysis of heterogeneous spatial distribution of Arabidopsis leaf trichomes using micro x-ray computed tomography. The Plant Journal 56, 470–482.
| Quantitative analysis of heterogeneous spatial distribution of Arabidopsis leaf trichomes using micro x-ray computed tomography.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVGmtbvP&md5=d38ebff32a142cd82f7c972090136028CAS |
Keller MM, Jaillais Y, Pedmale UV, Moreno JE, Chory J, Ballaré CL (2011) Cryptochrome 1 and phytochrome B control shade-avoidance responses in Arabidopsis via partially independent hormonal cascades. The Plant Journal 67, 195–207.
| Cryptochrome 1 and phytochrome B control shade-avoidance responses in Arabidopsis via partially independent hormonal cascades.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpvVSjsrw%3D&md5=119ec6ab86606d3d1f760850da24e422CAS |
Keuskamp DH, Sasidharan R, Vos I, Peeters AJM, Voesenek LACJ, Pierik R (2011) Blue light-mediated shade avoidance requires combined auxin and brassinosteroid action in Arabidopsis seedlings. The Plant Journal 67, 208–217.
| Blue light-mediated shade avoidance requires combined auxin and brassinosteroid action in Arabidopsis seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpvVSjsr0%3D&md5=de263b5a5c1d757117c19c1564a87169CAS |
Koini MA, Alvey L, Allen T, Tilley CA, Harberd NP, Whitelam GC, Franklin KA (2009) High temperature-mediated adaptations in plant architecture require the bHLH transcription factor PIF4. Current Biology 19, 408–413.
| High temperature-mediated adaptations in plant architecture require the bHLH transcription factor PIF4.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXivVKitbo%3D&md5=8ceab913782737713ee226611991d7fdCAS |
Lee K, Avondo J, Morrison H, Blot L, Stark M, Sharpe J, Bangham A, Coen E (2006) Visualizing plant development and gene expression in three dimensions using optical projection tomography. The Plant Cell 18, 2145–2156.
| Visualizing plant development and gene expression in three dimensions using optical projection tomography.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVKgurjF&md5=2423b14cfc772d0e43b9b8b0c0f377bfCAS |
Lorrain S, Allen T, Duek PD, Whitelam GC, Fankhauser C (2008) Phytochrome-mediated inhibition of shade avoidance involves degradation of growth-promoting bHLH transcription factors. The Plant Journal 53, 312–323.
| Phytochrome-mediated inhibition of shade avoidance involves degradation of growth-promoting bHLH transcription factors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFeht7g%3D&md5=3d1066c779a43902f42531bd1069a86aCAS |
Medina E, Sobrado M, Herrera R (1978) Significance of leaf orientation for leaf temperature in an Amazonian sclerophyll vegetation. Radiation and Environmental Biophysics 15, 131–140.
| Significance of leaf orientation for leaf temperature in an Amazonian sclerophyll vegetation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE1M%2FnsFCmsw%3D%3D&md5=7f686403b6a854ae4afa329801686575CAS |
Millar AJ, Straume M, Chory J, Chua NH, Kay SA (1995) The regulation of circadian period by phototransduction pathways in Arabidopsis. Science 267, 1163–1166.
| The regulation of circadian period by phototransduction pathways in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXktVKjsb8%3D&md5=7902ca224a2f4f9b0d6030fc87358555CAS |
Millenaar F, Cox M, van Berkel Y (2005) Ethylene-induced differential growth of petioles in Arabidopsis. Analyzing natural variation, response kinetics, and regulation. Plant Physiology 137, 998–1008.
| Ethylene-induced differential growth of petioles in Arabidopsis. Analyzing natural variation, response kinetics, and regulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXislOqsro%3D&md5=9250fce3454b73b9641e07953ab5a302CAS |
Millenaar F, van Zanten M, Cox M (2009) Differential petiole growth in Arabidopsis thaliana: photocontrol and hormonal regulation. New Phytologist 184, 141–152.
| Differential petiole growth in Arabidopsis thaliana: photocontrol and hormonal regulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1Kitb7J&md5=80f2431679e04f389144cf74b9436b7aCAS |
Moreno JE, Tao Y, Chory J, Ballaré CL (2009) Ecological modulation of plant defense via phytochrome control of jasmonate sensitivity. Proceedings of the National Academy of Sciences of the United States of America 106, 4935–4940.
| Ecological modulation of plant defense via phytochrome control of jasmonate sensitivity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXktFOjur4%3D&md5=106972588c91e603bb4304b045fd7e48CAS |
Mullen JL, Weinig C, Hangarter RP (2006) Shade avoidance and the regulation of leaf inclination in Arabidopsis. Plant, Cell & Environment 29, 1099–1106.
| Shade avoidance and the regulation of leaf inclination in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XlvFakur0%3D&md5=4101226271e75db58706f56ad174a727CAS |
Novoplansky A (2009) Picking battles wisely: plant behaviour under competition. Plant, Cell & Environment 32, 726–741.
| Picking battles wisely: plant behaviour under competition.Crossref | GoogleScholarGoogle Scholar |
Polko JK, van Zanten M, van Rooij JA, Marée AFM, Voesenek LACJ, Peeters AJM, Pierik R (2012) Ethylene-induced differential petiole growth in Arabidopsis thaliana involves local microtubule reorientation and cell expansion. New Phytologist 193, 339–348.
| Ethylene-induced differential petiole growth in Arabidopsis thaliana involves local microtubule reorientation and cell expansion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XitVejs7g%3D&md5=391dd4e30295f73d154986ab0c380b40CAS |
Salter MG, Franklin KA, Whitelam GC (2003) Gating of the rapid shade-avoidance response by the circadian clock in plants. Nature 426, 680–683.
| Gating of the rapid shade-avoidance response by the circadian clock in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXps1CksrY%3D&md5=53917eed13ae1ea77edb7d29b79fbfeeCAS |
Sasidharan R, Chinnappa CC, Staal M, Elzenga JTM, Yokoyama R, Nishitani K, Voesenek LACJ, Pierik R (2010) Light quality-mediated petiole elongation in Arabidopsis during shade avoidance involves cell wall modification by xyloglucan endotransglucosylase/hydrolases. Plant Physiology 154, 978–990.
| Light quality-mediated petiole elongation in Arabidopsis during shade avoidance involves cell wall modification by xyloglucan endotransglucosylase/hydrolases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlCkt7bO&md5=c6a3cf620947e61b681980bcee29b743CAS |
Sultan SE (2010) Plant developmental responses to the environment: eco-devo insights. Current Opinion in Plant Biology 13, 96–101.
| Plant developmental responses to the environment: eco-devo insights.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpslegug%3D%3D&md5=09b3b8342cb967171e441ff09926de66CAS |
Tao Y, Ferrer J-L, Ljung K, Pojer F, Hong F, Long JA, Li L, Moreno JE, Bowman E, Ivans LJ, Cheng Y, Lim J, Zhao Y, Ballaré CL, Sandberg G, Noel JP, Chory J (2008) Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell 133, 164–176.
| Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXkslOks7o%3D&md5=225b57e224f9468546768a5461d2d935CAS |
van Zanten M, Pons T, Janssen J (2010) On the relevance and control of leaf angle. Critical Reviews in Plant Sciences 29, 300–316.
| On the relevance and control of leaf angle.Crossref | GoogleScholarGoogle Scholar |
Voesenek LACJ, Colmer TD, Pierik R, Millenaar FF, Peeters AJM (2006) How plants cope with complete submergence. New Phytologist 170, 213–226.
| How plants cope with complete submergence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XltFamtLw%3D&md5=deda5e14ade66ba3829c2f101ddc387eCAS |
Wiese A, Christ MM, Virnich O, Schurr U, Walter A (2007) Spatio-temporal leaf growth patterns of Arabidopsis thaliana and evidence for sugar control of the diel leaf growth cycle. New Phytologist 174, 752–761.
| Spatio-temporal leaf growth patterns of Arabidopsis thaliana and evidence for sugar control of the diel leaf growth cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXnt1amtL8%3D&md5=31557f3a8f914af45b6e1b4698a1a059CAS |
